Vaccination with human papillomavirus pseudovirus-encapsidated plasmids targeted to skin using microneedles

PLoS ONE

Volumn 10, Issue 3, 2015, Pages

  Kines, Rhonda C ^a,d   Zarnitsyn, Vladimir ^b   Johnson, Teresa R ^c   Pang, Yuk Ying S ^a   Corbett, Kizzmekia S ^c   Nicewonger, John D ^c   Gangopadhyay, Anu ^c   Chen, Man ^c   Liu, Jie ^c   Prausnitz, Mark R ^b   Schiller, John T ^a   Graham, Barney S ^c  

^a NATIONAL CANCER INSTITUTE   (United States)

^b Georgia Institute of Technology   (United States)

^c NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

^d Aura Biosciences   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ENCAPSIDATED PLASMID; HUMAN PAPILLOMA VIRUS 16 VIRUS LIKE PARTICLE VACCINE; HUMAN PAPILLOMA VIRUS 16 VIRUS PSEUDOVIRION VACCINE; PLASMID DNA; UNCLASSIFIED DRUG; VIRUS LIKE PARTICLE VACCINE; WART VIRUS VACCINE; LUCIFERASE; MATRIX PROTEIN; NEUTRALIZING ANTIBODY; VIRUS ANTIBODY; VIRUS DNA; VIRUS FUSION PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTIBODY RESPONSE; ANTIBODY TITER; ARTICLE; B LYMPHOCYTE; CD3+ T LYMPHOCYTE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELLULAR IMMUNITY; CONTROLLED STUDY; DOSE RESPONSE; DRUG EFFICACY; DRUG MEGADOSE; FEMALE; HUMAN PAPILLOMAVIRUS TYPE 16; HUMAN PAPILLOMAVIRUS TYPE 2; HUMAN RESPIRATORY SYNCYTIAL VIRUS; IMMUNOGENICITY; INTERMETHOD COMPARISON; LOW DRUG DOSE; MICRONEEDLE; MOUSE; NONHUMAN; PAPILLOMAVIRUS INFECTION; VACCINATION; VIRUS LOAD; WART VIRUS; ADMINISTRATION AND DOSAGE; ANIMAL; BIOSYNTHESIS; CUTANEOUS DRUG ADMINISTRATION; DRUG EFFECTS; GENE EXPRESSION; GENETICS; HUMAN; IMMUNOLOGY; METABOLISM; MICROINJECTION; NEEDLE; PAPILLOMAVIRUS INFECTIONS; PLASMID; REPORTER GENE; SKIN; TRANSGENE; UTERINE CERVICAL NEOPLASMS; VIROLOGY;

HUMAN PAPILLOMAVIRUS; MIRIDAE; MUS; RESPIRATORY SYNCYTIAL VIRUS; RICE STRIPE VIRUS;

ADMINISTRATION, CUTANEOUS; ANIMALS; ANTIBODIES, NEUTRALIZING; ANTIBODIES, VIRAL; DNA, VIRAL; FEMALE; GENE EXPRESSION; GENES, REPORTER; HUMAN PAPILLOMAVIRUS 16; HUMANS; LUCIFERASES; MICE; MICROINJECTIONS; NEEDLES; PAPILLOMAVIRUS INFECTIONS; PAPILLOMAVIRUS VACCINES; PLASMIDS; RESPIRATORY SYNCYTIAL VIRUSES; SKIN; TRANSGENES; UTERINE CERVICAL NEOPLASMS; VACCINATION; VACCINES, VIRUS-LIKE PARTICLE; VIRAL FUSION PROTEINS; VIRAL MATRIX PROTEINS;

EID: 84925425840     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0120797     Document Type: Article

References (46)

1. Nestle FO, Di Meglio P, Qin JZ, Nickoloff BJ. Skin immune sentinels in health and disease. Nat Rev Immunol. 2009 Oct; 9(10):679-91 doi: 101038/nri2622 Epub 2009 Sep 18. PMID: 19763149
2. Kim YC, Park JH, Prausnitz MR. Microneedles for drug and vaccine delivery. Adv Drug Deliv Rev 2012 Nov; 64(14):1547-68 doi: 101016/jaddr201204005 Epub 2012 May 1. PMID: 22575858
3. Gill HS, Soderholm J, Prausnitz MR, Sallberg M. Cutaneous vaccination using microneedles coated with hepatitis C DNA vaccine. Gene Ther. 2010 Jun; 17(6):811-4 doi: 101038/gt201022 Epub 2010 Mar 4. PMID: 20200562
4. Gonzalez-Gonzalez E, Kim Y-C, Speaker TJ, Hickerson RP, Spitler R, Birchall JC, et al. Visualization of plasmid delivery to keratinocytes in mouse and human epidermis. Sci Rep 1. 2011; 1:158.
5. Pearton M, Saller V, Coulman SA, Gateley C, Anstey AV, Zarnitsyn V, et al. Microneedle delivery of plasmid DNA to living human skin: Formulation coating, skin insertion and gene expression. J Control Release. 2012 Jun 28; 160(3):561-9 doi: 101016/jjconrel201204005 Epub 2012 Apr 10. PMID: 22516089
6. Song JM, Kim YC, O E, Compans RW, Prausnitz MR, Kang SM. DNA vaccination in the skin using microneedles improves protection against influenza. Mol Ther. 2012 Jul; 20(7):1472-80 doi: 101038/mt201269 Epub 2012 Apr 17. PMID: 22508490
7. Quan FS, Kim YC, Vunnava A, Yoo DG, Song JM, Prausnitz MR, et al. Intradermal vaccination with influenza virus-like particles by using microneedles induces protection superior to that with intramuscular immunization. J Virol. 2010 Aug; 84(15):7760-9 doi: 101128/JVI01849-09 Epub 2010 May 19. PMID: 20484519
8. Song JM, Kim YC, Lipatov AS, Pearton M, Davis CT, Yoo DG, et al. Microneedle delivery of H5N1 influenza virus-like particles to the skin induces long-lasting B- and T-cell responses in mice. Clin Vaccine Immunol. 2010 Sep; 17(9):1381-9 doi: 101128/CVI00100-10 Epub 2010 Jul 14. PMID: 20631330
9. Corbett HJ, Fernando GJ, Chen X, Frazer IH, Kendall MA. Skin vaccination against cervical cancer associated human papillomavirus with a novel micro-projection array in a mouse model. PLoS One. 2010 Oct 18; 5(10):e13460 doi: 101371/journalpone0013460 PMID: 20976136
10. Bachy V, Hervouet C, Becker PD, Chorro L, Carlin LM, Herath S, et al. Langerin negative dendritic cells promote potent CD8+ T-cell priming by skin delivery of live adenovirus vaccine microneedle arrays. Proc Natl Acad Sci U S A. 2013 Feb 19; 110(8):3041-6 doi: 101073/pnas1214449110 Epub 2013 Feb 5. PMID: 23386724
11. Edens C, Collins ML, Ayers J, Rota PA, Prausnitz MR. Measles vaccination using a microneedle patch. Vaccine. 2013; 31(34):3403-9. doi: 10.1016/j.vaccine.2012.09.062 PMID: 23044406
12. de Sanjose S, Quint WGV, Alemany L, Geraets DT, Klaustermeier JE, Lloveras B, et al. Human papillomavirus genotype attribution in invasive cervical cancer: a retrospective cross-sectional worldwide study. The Lancet Oncology. 2010; 11: 1048-1056. doi: 10.1016/S1470-2045(10)70230-8 PMID: 20952254
13. Ferlay J, Shin H-R, Bray F, Forman D, Mathers C, Parkin DM. Estimates of worldwide burden of cancer in 2008: GLOBOCAN 2008. Int J Canc. 2010; 127: 2893-2917. doi: 10.1002/ijc.25516 PMID: 21351269
14. de Martel C, Ferlay J, Franceschi S, Vignat Jrm, Bray F, Forman D, et al. Global burden of cancers attributable to infections in 2008: a review and synthetic analysis. The Lancet Oncology. 2012; 13: 607-615. doi: 10.1016/S1470-2045(12)70137-7 PMID: 22575588
15. Hopkins TG, Wood N. Female human papillomavirus (HPV) vaccination: Global uptake and the impact of attitudes. Vaccine. 2012; 31: 1673-1679.
16. Hall CB, Weinberg GA, Iwane MK, Blumkin AK, Edwards KM, Staat MA, et al. The burden of respiratory syncytial virus infection in young children. N Engl J Med. 2009 Feb 5; 360(6):588-98 doi: 101056/NEJMoa0804877 PMID: 19196675
17. Stockman LJ, Curns AT, Anderson LJ, Fischer-Langley G. Respiratory syncytial virus-associated hospitalizations among infants and young children in the United States, 1997-2006. Pediatr Infect Dis J. 2012 Jan; 31(1):5-9 doi: 101097/INF0b013e31822e68e6 PMID: 21817948
18. Johnson S, Oliver C, Prince GA, Hemming VG, Pfarr DS, Wang SC, et al. Development of a Humanized Monoclonal Antibody (MEDI-493) with Potent In Vitro and In Vivo Activity against Respiratory Syncytial Virus. J Infect Dis. 1997; 176: 1215-1224. PMID: 9359721
19. Meissner HC, Welliver RC, Chartrand SA, Law BJ, Weisman LE, Dorkin HL, et al. Immunoprophylaxis with palivizumab, a humanized respiratory syncytial virus monoclonal antibody, for prevention of respiratory syncytial virus infection in high risk infants: a consensus opinion. Pediatr Infect Dis J. 1999 Mar; 18(3):223-31. PMID: 10093942
20. Beeler JA, van Wyke Coelingh K. Neutralization epitopes of the F glycoprotein of respiratory syncytial virus: effect of mutation upon fusion function. J Virol. 1989 Jul; 63(7):2941-50. PMID: 2470922
21. McLellan JS, Chen M, Leung S, Graepel KW, Du X, Yang Y, et al. Structure of RSV fusion glycoprotein trimer bound to a prefusion-specific neutralizing antibody. Science. 2013 May 31; 340(6136):1113-7 doi: 101126/science1234914 Epub 2013 Apr 25. PMID: 23618766
22. Graham BS, Walker C. Meeting the Challenge of Vaccine Design to Control HIV and Other Difficult Viruses. In Rouse BT, Kaufmann SHE, Sacks DL, editors. The Immune Response to Infection. Washington D.C: ASM; 2011. pp 559-570.
23. Buck CB, Thompson CD. Production of papillomavirus-based gene transfer vectors. Curr Protoc Cell Biol. 2007 Dec;Chapter 26:Unit 261 doi: 101002/0471143030cb2601s37
24. Graham BS, Kines RC, Corbett KS, Nicewonger J, Johnson TR, Chen M, et al. Mucosal delivery of human papillomavirus pseudovirus-encapsidated plasmids improves the potency of DNA vaccination. Mucosal Immunol. 2010 Sep; 3(5):475-86 doi: 101038/mi201031 Epub 2010 Jun 16. PMID: 20555315
25. Gordon SN, Kines RC, Kutsyna G, Ma ZM, Hryniewicz A, Roberts JN, et al. Targeting the vaginal mucosa with human papillomavirus pseudovirion vaccines delivering simian immunodeficiency virus DNA. J Immunol. 2012 Jan 15; 188(2):714-23 doi: 104049/jimmunol1101404 Epub 2011 Dec 14. PMID: 22174446
26. Cuburu N, Graham BS, Buck CB, Kines RC, Pang YY, Day PM, et al. Intravaginal immunization with HPV vectors induces tissue-resident CD8+ T cell responses. J Clin Invest. 2012 Dec 3; 122(12):4606-20 doi: 101172/JCI63287 Epub 2012 Nov 12. PMID: 23143305
27. Gill HS, Prausnitz MR. Coated microneedles for transdermal delivery. J Control Release. 2007 Feb 12; 117(2):227-37 Epub 2006 Oct 24. PMID: 17169459
28. Graham BS, Perkins MD, Wright PF, Karzon DT. Primary respiratory syncytial virus infection in mice. J Med Virol. 1988 Oct; 26(2):153-62. PMID: 3183639
29. Johnson TR, Johnson JE, Roberts SR, Wertz GW, Parker RA, Graham BS. Priming with secreted glycoprotein G of respiratory syncytial virus (RSV) augments interleukin-5 production and tissue eosinophilia after RSV challenge. J Virol. 1998 Apr; 72(4):2871-80. PMID: 9525607
30. Pastrana DV, Buck CB, Pang YY, Thompson CD, Castle PE, FitzGerald PC, et al. Reactivity of human sera in a sensitive, high-throughput pseudovirus-based papillomavirus neutralization assay for HPV16 and HPV18. Virology. 2004 Apr 10; 321(2):205-16. PMID: 15051381
31. McLellan JS, Yang Y, Graham BS, Kwong PD. Structure of Respiratory Syncytial Virus Fusion Glycoprotein in the Postfusion Conformation Reveals Preservation of Neutralizing Epitopes. J Virol. 2011; 85: 7788-7796. doi: 10.1128/JVI.00555-11 PMID: 21613394
32. Rutigliano JA, Ruckwardt TJ, Martin JE, Graham BS. Relative dominance of epitope-specific CD8+ T cell responses in an F1 hybrid mouse model of respiratory syncytial virus infection. Virology. 2007; 362: 314-319. PMID: 17275872
33. Roberts JN, Buck CB, Thompson CD, Kines R, Bernardo M, Choyke PL, et al. Genital transmission of HPV in a mouse model is potentiated by nonoxynol-9 and inhibited by carrageenan. Nat Med. 2007 Jul; 13(7):857-61 Epub 2007 Jul 1. PMID: 17603495
34. Mitsunaga M, Kosaka N, Kines RC, Roberts JN, Lowy DR, Schiller JT, et al. In vivo longitudinal imaging of experimental human papillomavirus infection in mice with a multicolor fluorescence mini-endoscopy system. Cancer Prev Res. 2011 May; 4(5):767-73 doi: 101158/1940-6207CAPR-10-0334 Epub 2011 Mar 23.
35. Liu J, Ruckwardt TJ, Chen M, Johnson TR, Graham BS. Characterization of respiratory syncytial virus M- and M2-specific CD4 T cells in a murine model. J Virol. 2009 May; 83(10):4934-41 doi: 101128/JVI02140-08 Epub 2009 Mar 4. PMID: 19264776
36. Ledgerwood JE, Wei CJ, Hu Z, Gordon IJ, Enama ME, Hendel CS, et al. DNA priming and influenza vaccine immunogenicity: two phase 1 open label randomised clinical trials. Lancet Infect Dis. 2011; 11: 916-924. doi: 10.1016/S1473-3099(11)70240-7 PMID: 21975270
37. Ledgerwood JE, Zephir K, Hu Z, Wei CJ, Chang L, Enama ME, et al. Prime-boost interval matters: a randomized phase 1 study to identify the minimum interval necessary to observe the H5 DNA influenza vaccine priming effect. J Infect Dis. 2013; 208: 418-422. doi: 10.1093/infdis/jit180 PMID: 23633407
38. Khurana S, Wu J, Dimitrova M, King LR, Manischewitz J, Graham BS, et al. DNA priming prior to inactivated influenza A(H5N1) vaccination expands the antibody epitope repertoire and increases affinity maturation in a boost-interval-dependent manner in adults. J Infect Dis. 2013; 208: 413-417. doi: 10.1093/infdis/jit178 PMID: 23633404
39. Kenney RT, Frech SA, Muenz LR, Villar CP, Glenn GM. Dose sparing with intradermal injection of influenza vaccine. N Engl J Med. 2004 Nov 25; 351(22):2295-301 Epub 2004 Nov 3. PMID: 15525714
40. Sheets RL, Stein J, Manetz TS, Duffy C, Nason M, Andrews C, et al. Biodistribution of DNA Plasmid Vaccines against HIV-1, Ebola, Severe Acute Respiratory Syndrome, or West Nile Virus Is Similar, without Integration, despite Differing Plasmid Backbones or Gene Inserts. Toxicol Sci. 2006; 91: 610-619. PMID: 16569729
41. 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: 1396-1404. doi: 10.1093/infdis/jir054 PMID: 21398392
42. Graham BS, Enama ME, Nason MC, Gordon IJ, Peel SA, Ledgerwood JE, et al. DNA vaccine delivered by a needle-free injection device improves potency of priming for antibody and CD8+ T-cell responses after rAd5 boost in a randomized clinical trial. PLoS One. 2013; 8(4):e59340. doi: 10.1371/journal.pone.0059340 PMID: 23577062
43. Favard C, Dean DS, Rols MP. Electrotransfer as a non viral method of gene delivery. Curr Gene Ther. 2007 Feb; 7(1):67-77. PMID: 17305529
44. Hirao LA, Wu L, Satishchandran A, Khan AS, Draghia-Akli R, Finnefrock AC, et al. Comparative analysis of immune responses induced by vaccination with SIV antigens by recombinant Ad5 vector or plasmid DNA in rhesus macaques. Mol Ther. 2010 Aug; 18(8):1568-76 doi: 101038/mt2010112 Epub 2010 Jun 15. PMID: 20551910
45. Vasan S, Hurley A, Schlesinger SJ, Hannaman D, Gardiner DF, Dugin DP, et al. In vivo electroporation enhances the immunogenicity of an HIV-1 DNA vaccine candidate in healthy volunteers. PLoS One. 2011; 6(5):e19252. doi: 10.1371/journal.pone.0019252 PMID: 21603651
46. Sullivan SP, Koutsonanos DG, Del Pilar Martin M, Lee JW, Zarnitsyn V, Choi SO, et al. Dissolving polymer microneedle patches for influenza vaccination. Nat Med. 2010 Aug; 16(8):915-20 doi: 101038/nm2182 Epub 2010 Jul 18. PMID: 20639891