VLPs and particle strategies for cancer vaccines

Expert Review of Vaccines

Volumn 12, Issue 10, 2013, Pages 1173-1193

  Ungaro, Francesca ^a   Conte, Claudia ^a   Quaglia, Fabiana ^a   Tornesello, Maria Lina ^b   Buonaguro, Franco M ^b   Buonaguro, Luigi ^b  

^a UNIVERSITY OF NAPLES FEDERICO II   (Italy)

^b NATIONAL CANCER INSTITUTE   (Italy)

Author keywords

antigen presenting cells; cancer vaccines; HBV; HPV; ISCOMs; liposomes; nanoparticles; polymers; virus like particles

Indexed keywords

CANCER VACCINE; CHITOSAN; EMEPEPIMUT S; HEPATITIS B VACCINE; ISCOM; LIPID; LIPOSOME; NANOPARTICLE; POLYAMINOACID; POLYESTER;

CANCER IMMUNOTHERAPY; CELLULAR IMMUNITY; DRUG DELIVERY SYSTEM; DRUG DESIGN; HEPATITIS B VIRUS; HUMAN; HUMORAL IMMUNITY; IMMUNOGENICITY; LIPID VESICLE; NONHUMAN; PAPILLOMA VIRUS; POLYMERIZATION; PRIORITY JOURNAL; REVIEW; STATIC ELECTRICITY; TECHNOLOGY; VIRUS LIKE AGENT;

ANTIGENS, NEOPLASM; CANCER VACCINES; DRUG CARRIERS; HUMANS; LIPOSOMES; NANOPARTICLES; NEOPLASMS; VACCINATION; VACCINES, VIRUS-LIKE PARTICLE; VIRUSES;

EID: 84886071009     PISSN: 14760584     EISSN: 17448395     Source Type: Journal    
DOI: 10.1586/14760584.2013.836909     Document Type: Review

References (204)

1. De Temmerman ML, Rejman J, Demeester J, Irvine DJ, Gander B, De Smedt SC. Particulate vaccines: on the quest for optimal delivery and immune response. Drug Discov. Today 16(13-14), 569-582 (2011).
2. Moon JJ, Huang B, Irvine DJ. Engineering nano-and microparticles to tune immunity. Adv. Mater. 24(28), 3724-3746 (2012).
3. Joshi MD, Unger WJ, Storm G, van Kooyk Y, Mastrobattista E. Targeting tumor antigens to dendritic cells using particulate carriers. J. Control. Release 161(1), 25-37 (2012).
4. Sharp FA, Ruane D, Claass B et al. Uptake of particulate vaccine adjuvants by dendritic cells activates the NALP3 inflammasome. Proc. Natl Acad. Sci. USA 106(3), 870-875 (2009).
5. Demento SL, Eisenbarth SC, Foellmer HG et al. Inflammasome-activating nanoparticles as modular systems for optimizing vaccine efficacy. Vaccine 27(23), 3013-3021 (2009).
6. Ghiringhelli F, Apetoh L, Tesniere A et al. Activation of the NLRP3 inflammasome in dendritic cells induces IL-1beta-dependent adaptive immunity against tumors. Nat. Med. 15(10), 1170-1178 (2009).
7. Salvador A, Igartua M, Hernandez RM, Pedraz JL. An overview on the field of micro-and nanotechnologies for synthetic Peptide-based vaccines. J. Drug Deliv. 2011, 181646 (2011).
8. Delchambre M, Gheysen D, Thines D et al. The GAG precursor of simian immunodeficiency virus assembles into virus-like particles. EMBO J. 8(9), 2653-2660 (1989). (Pubitemid 19273350)
9. Miyanohara A, Imamura T, Araki M, Sugawara K, Ohtomo N, Matsubara K. Expression of hepatitis B virus core antigen gene in Saccharomyces cerevisiae: synthesis of two polypeptides translated from different initiation codons. J. Virol. 59, 176-180 (1986). (Pubitemid 16062513)
10. Malboeuf CM, Simon DA, Lee YE et al. Human papillomavirus-like particles mediate functional delivery of plasmid DNA to antigen presenting cells in vivo. Vaccine 25(17), 3270-3276 (2007). (Pubitemid 46527999)
11. Touze A, Coursaget P. In vitro gene transfer using human papillomavirus-like particles. Nucleic Acids Res. 26(5), 1317-1323 (1998). (Pubitemid 28291707)
12. Buonaguro FM, Tornesello ML, Buonaguro L. Virus-like particle vaccines and adjuvants: the HPV paradigm. Expert. Rev.Vaccines 8(10), 1379-1398 (2009).
13. Xu YF, Zhang YQ, Xu XM, Song GX. Papillomavirus virus-like particles as vehicles for the delivery of epitopes or genes. Arch. Virol. 151(11), 2133-2148 (2006).
14. Bachmann MF, Lutz MB, Layton GT et al. Dendritic cells process exogenous viral proteins and virus-like particles for class I presentation to CD8+ cytotoxic T lymphocytes. Eur. J. Immunol. 26(11), 2595-2600 (1996). (Pubitemid 26364834)
15. Ruedl C, Storni T, Lechner F, Bachi T, Bachmann MF. Cross-presentation of virus-like particles by skin-derived CD8(-) dendritic cells: a dispensable role for TAP. Eur. J. Immunol. 32(3), 818-825 (2002). (Pubitemid 34257559)
16. Buonaguro L, Tornesello ML, Buonaguro FM. Virus-like particles as particulate vaccines. Curr. HIV Res. 8(4), 299-309. (2010).
17. Kirnbauer R, Booy F, Cheng N, Lowy DR, Schiller JT. Papillomavirus L1 major capsid protein self-assembles into virus-like particles that are highly immunogenic. Proc. Natl Acad. Sci. USA 89, 12180-12184 (1992). (Pubitemid 23004809)
18. Lopez de Turiso JA, Cortes E, Martinez C et al. Recombinant vaccine for canine parvovirus in dogs. J. Virol. 66(5), 2748-2753 (1992).
19. Brautigam S, Snezhkov E, Bishop DH. Formation of poliovirus-like particles by recombinant baculoviruses expressing the individual VP0, VP3, and VP1 proteins by comparison to particles derived from the expressed poliovirus polyprotein. Virology 192(2), 512-524 (1993).
20. Kozlovska TM, Cielens I, Dreilinna D et al. Recombinant RNA phage Q beta capsid particles synthesized and self-assembled in Escherichia coli. Gene 137(1), 133-137 (1993). (Pubitemid 24053742)
21. Baumert TF, Ito S, Wong DT, Liang TJ. Hepatitis C virus structural proteins assemble into viruslike particles in insect cells. J. Virol. 72, 3827-36. (1998). (Pubitemid 28188682)
22. McAleer WJ, Buynak EB, Maigetter RZ, Wampler DE, Miller WJ, Hilleman MR. Human hepatitis B vaccine from recombinant yeast. Nature 307(5947), 178-180 (1984). (Pubitemid 14132908)
23. Kang SM, Song JM, Quan FS, Compans RW. Influenza vaccines based on virus-like particles. Virus Res. 143(2), 140-146 (2009).
24. Buonaguro L, Buonaguro FM, Tornesello ML et al. High efficient production of Pr55gag Virus-like Particles expressing multiple HIV-1 epitopes, including a gp120 protein derived from an Ugandan HIV-1 isolate of subtype A. Antiviral Res. 49, 35-47 (2001). (Pubitemid 32146577)
25. Gheysen D, Jacobs E, de Foresta F et al. Assembly and release of HIV-1 precursor Pr55gag virus-like particles from recombinant baculovirus-infected insect cells. Cell 59, 103-112 (1989). (Pubitemid 19248562)
26. Wang BZ, Liu W, Kang SM et al. Incorporation of high levels of chimeric human immunodeficiency virus envelope glycoproteins into virus-like particles. J. Virol. 81(20), 10869-10878 (2007). (Pubitemid 47536061)
27. Tobin GJ, Li GH, Fong SE, Nagashima K, Gonda MA. Chimeric HIV-1 virus-like particles containing gp120 epitopes as a result of a ribosomal frameshift elicit gagand SU-specific murine cytotoxic T-lymphocyte activities. Virology 236, 307-315 (1997). (Pubitemid 27423773)
28. Griffiths JC, Harris SJ, Layton GT et al. Hybrid human immunodeficiency virus Gag particles as an antigen carrier system: Induction of cytotoxic T-cell and humoral responses by a Gag:V3 fusion. J. Virol. 67, 3191-3198 (1993). (Pubitemid 23143689)
29. Schmitz N, Dietmeier K, Bauer M et al. Displaying Fel d1 on virus-like particles prevents reactogenicity despite greatly enhanced immunogenicity: a novel therapy for cat allergy. J. Exp. Med. 206(9), 1941-1955 (2009).
30. Bachmann MF, Jennings GT. Therapeutic vaccines for chronic diseases: successes and technical challenges. Philos. Trans. R Soc. Lond B Biol. Sci. 366(1579), 2815-2822 (2011).
31. Moron VG, Rueda P, Sedlik C, Leclerc C. In vivo, dendritic cells can cross-present virus-like particles using an endosome-to-cytosol pathway. J. Immunol. 171, 2242-2250 (2003). (Pubitemid 37025529)
32. Moron G, Rueda P, Casal I, Leclerc C. CD8alpha-CD11b+ dendritic cells present exogenous virus-like particles to CD8+ T cells and subsequently express CD8alpha and CD205 molecules. J. Exp. Med. 195(10), 1233-1245 (2002). (Pubitemid 34564326)
33. Buonaguro L, Tornesello ML, Tagliamonte M et al. Baculovirus-derived human immunodeficiency virus type 1 virus-like particles activate dendritic cells and induce ex vivo T-cell responses. J. Virol. 80, 9134-9143 (2006). (Pubitemid 44362963)
34. Buonaguro L, Tornesello ML, Gallo RC, Marincola FM, Lewis GK, Buonaguro FM. Th2 polarization in peripheral blood mononuclear cells from human immunodeficiency virus (HIV)-infected subjects, as activated by HIV virus-like particles. J. Virol. 83(1), 304-313 (2009).
35. Tsunetsugu-Yokota Y, Morikawa Y, Isogai M et al. Yeast-derived human immunodeficiency virus type 1 p55gag virus-like particles activate dendritic cells (DCs) and induce perforin expression in gag-specific CD8+ T cells by cross-presentation of DCs. J. Virol. 77, 10250-10259 (2003). (Pubitemid 37129668)
36. Lenz P, Thompson CD, Day PM, Bacot SM, Lowy DR, Schiller JT. Interaction of papillomavirus virus-like particles with human myeloid antigen-presenting cells. Clin. Immunol. 106, 231-237 (2003). (Pubitemid 36428995)
37. Bachmann MF, Kundig TM, Kalberer CP, Hengartner H, Zinkernagel RM. Formalin inactivation of vesicular stomatitis virus impairs T-cell-but not T-help-independent B-cell responses. J. Virol. 67(7), 3917-3922 (1993). (Pubitemid 23180715)
38. Braciale TJ, Morrison LA, Sweetser MT, Sambrook J, Gething MJ, Braciale VL. Antigen presentation pathways to class I and class II MHC-restricted T lymphocytes. Immunol. Rev. 98, 95-114 (1987). (Pubitemid 17128067)
39. Paliard X, Liu Y, Wagner R, Wolf H, Baenzinger J, Walker CM. Priming of strong, broad, and long-lived HIV type 1 p55gag-specific CD8+ cytotoxic T cells after administration of a virus-like particle vaccine in rhesus macaques. AIDS Res. Hum. Retroviruses 16, 273-282 (2000). (Pubitemid 30111963)
40. Buonaguro L, Racioppi L, Tornesello ML et al. Induction of neutralizing antibodies and CTLs in Balb/c mice immunized with Virus-like Particles presenting a gp120 molecule from a HIV-1 isolate of clade A (HIV-VLPAs). Antiviral Res. 54, 189-201 (2002). (Pubitemid 34327684)
41. Buonaguro L, Visciano ML, Tornesello ML, Tagliamonte M, Biryahwaho B, Buonaguro FM. Induction of systemic and mucosal cross-clade neutralizing antibodies in BALB/c mice immunized with human immunodeficiency virus type 1 clade A virus-like particles administered by different routes of inoculation. J. Virol. 79, 7059-7067 (2005). (Pubitemid 40677337)
42. Buonaguro L, Devito C, Tornesello ML et al. DNA-VLP prime-boost intra-nasal immunization induces cellular and humoral anti-HIV-1 systemic and mucosal immunity with cross-clade neutralizing activity. Vaccine 25(32), 5968-5977 (2007). (Pubitemid 47082465)
43. Manolova V, Flace A, Bauer M, Schwarz K, Saudan P, Bachmann MF. Nanoparticles target distinct dendritic cell populations according to their size. Eur. J. Immunol. 38(5), 1404-1413 (2008).
44. Hinton HJ, Jegerlehner A, Bachmann MF. Pattern recognition by B cells: the role of antigen repetitiveness versus Toll-like receptors. Curr. Top Microbiol. Immunol. 319, 1-15 (2008).
45. Bachmann MF, Rohrer UH, Kundig TM, Burki K, Hengartner H, Zinkernagel RM. The influence of antigen organization on B cell responsiveness. Science 262(5138), 1448-1451 (1993). (Pubitemid 24035067)
46. Aricò E, Wang E, Tornesello ML et al. Immature monocyte derived dendritic cells gene expression profile in response to Virus-Like Particles stimulation. J. Transl. Med. 3, 45.-(2005).
47. Buonaguro L, Monaco A, Arico E et al. Gene expression profile of peripheral blood mononuclear cells in response to HIV-VLPs stimulation. BMC Bionformatics 9(Suppl. 2), S5 (2008).
48. Monaco A, Marincola FM, Sabatino M et al. Molecular immune signatures of HIV-1 vaccines in human PBMCs. FEBS Lett. 583(18), 3004-3008 (2009).
49. Storni T, Ruedl C, Schwarz K, Schwendener RA, Renner WA, Bachmann MF. Nonmethylated CG motifs packaged into virus-like particles induce protective cytotoxic T cell responses in the absence of systemic side effects. J. Immunol. 172(3), 1777-1785 (2004). (Pubitemid 38116826)
50. Skountzou I, Quan FS, Gangadhara S et al. Incorporation of glycosylphosphatidylinositol-anchored granulocyte-macrophage colony-stimulating factor or CD40 ligand enhances immunogenicity of chimeric simian immunodeficiency virus-like particles. J. Virol. 81(3), 1083-1094 (2007). (Pubitemid 46167831)
51. Wang BZ, Quan FS, Kang SM, Bozja J, Skountzou I, Compans RW. Incorporation of membrane-anchored flagellin into influenza virus-like particles enhances the breadth of immune responses. J. Virol. 82(23), 11813-11823 (2008).
52. Schwarz K, Storni T, Manolova V et al. Role of Toll-like receptors in costimulating cytotoxic T cell responses. Eur. J. Immunol. 33(6), 1465-1470 (2003). (Pubitemid 36790406)
53. Sun S, Rao NL, Venable J, Thurmond R, Karlsson L. TLR7/9 antagonists as therapeutics for immune-mediated inflammatory disorders. Inflamm. Allergy Drug Targets. 6(4), 223-235 (2007).
54. Wampler DE, Lehman ED, Boger J, McAleer WJ, Scolnick EM. Multiple chemical forms of hepatitis B surface antigen produced in yeast. Proc. Natl Acad. Sci.USA 82(20), 6830-6834 (1985). (Pubitemid 16209654)
55. Valenzuela P, Medina A, Rutter WJ, Ammerer G, Hall BD. Synthesis and assembly of hepatitis B virus surface antigen particles in yeast. Nature 298(5872), 347-350 (1982). (Pubitemid 12044287)
56. Chang MH, Chen CJ, Lai MS et al. Universal hepatitis B vaccination in Taiwan and the incidence of hepatocellular carcinoma in children. Taiwan Childhood Hepatoma Study Group. N. Engl J. Med. 336(26), 1855-1859 (1997).
57. Wichajarn K, Kosalaraksa P, Wiangnon S. Incidence of hepatocellular carcinoma in children in Khon Kaen before and after national hepatitis B vaccine program. Asian Pac. J. Cancer Prev. 9(3), 507-509 (2008).
58. Lanier AP, Holck P, Ehrsam DG, Key C. Childhood cancer among Alaska Natives. Pediatrics 112(5), e396 (2003).
59. Pniewski T, Kapusta J, Bociag P et al. Low-dose oral immunization with lyophilized tissue of herbicide-resistant lettuce expressing hepatitis B surface antigen for prototype plant-derived vaccine tablet formulation. J. Appl. Genet. 52(2), 125-136 (2011).
60. Huang Z, Chen Q, Hjelm B, Arntzen C, Mason H. A DNA replicon system for rapid high-level production of virus-like particles in plants. Biotechnol. Bioeng. 103(4), 706-714 (2009).
61. Fernandez-San MA, Ortigosa SM, Hervas-Stubbs S et al. Human papillomavirus L1 protein expressed in tobacco chloroplasts self-assembles into virus-like particles that are highly immunogenic. Plant Biotechnol. J. 6(5), 427-441 (2008). (Pubitemid 351670277)
62. Maclean J, Koekemoer M, Olivier AJ et al. Optimization of human papillomavirus type 16 (HPV-16) L1 expression in plants: comparison of the suitability of different HPV-16 L1 gene variants and different cell-compartment localization. J. Gen. Virol. 88(Pt 5), 1460-1469 (2007). (Pubitemid 46723227)
63. Zhou J, Sun XY, Stenzel DJ, Frazer IH. Expression of vaccinia recombinant HPV 16 L1 and L2 ORF proteins in epithelial cells is sufficient for assembly of HPV virion-like particles. Virology 185(1), 251-257 (1991).
64. Lenzi P, Scotti N, Alagna F et al. Translational fusion of chloroplast-expressed human papillomavirus type 16 L1 capsid protein enhances antigen accumulation in transplastomic tobacco. Transgenic. Res. 17(6), 1091-1102 (2008).
65. Koutsky LA, Ault KA, Wheeler CM et al. A controlled trial of a human papillomavirus type 16 vaccine. N. Engl J. Med. 347, 1645-1651 (2002). (Pubitemid 35340782)
66. Evans TG, Bonnez W, Rose RC et al. A Phase 1 study of a recombinant viruslike particle vaccine against human papillomavirus type 11 in healthy adult volunteers. J. Infect. Dis. 183(10), 1485-1493 (2001). (Pubitemid 32417699)
67. Harro CD, Pang YY, Roden RB et al. Safety and immunogenicity trial in adult volunteers of a human papillomavirus 16 L1 virus-like particle vaccine. J. Natl Cancer Inst. 93(4), 284-292 (2001). (Pubitemid 32219815)
68. Harper DM, Franco EL, Wheeler CM et al. Sustained efficacy up to 4.5 years of a bivalent L1 virus-like particle vaccine against human papillomavirus types 16 and 18: follow-up from a randomised control trial. Lancet 367(9518), 1247-1255 (2006).
69. Paavonen J, Jenkins D, Bosch FX et al. Efficacy of a prophylactic adjuvanted bivalent L1 virus-like-particle vaccine against infection with human papillomavirus types 16 and 18 in young women: an interim analysis of a phase III double-blind, randomised controlled trial. Lancet 369(9580), 2161-2170 (2007). (Pubitemid 46977438)
70. Villa LL, Costa RL, Petta CA et al. High sustained efficacy of a prophylactic quadrivalent human papillomavirus types 6/11/16/18 L1 virus-like particle vaccine through 5 years of follow-up. Br. J. Cancer 95(11), 1459-1466 (2006). (Pubitemid 44863348)
71. The FUTURE II Study Group. Quadrivalent vaccine against human papillomavirus to prevent high-grade cervical lesions. N. Engl J. Med. 356(19), 1915-1927 (2007).
72. Giannini SL, Hanon E, Moris P et al. Enhanced humoral and memory B cellular immunity using HPV16/18 L1 VLP vaccine formulated with the MPL/aluminium salt combination (AS04) compared to aluminium salt only. Vaccine 24(33-34), 5937-5949 (2006). (Pubitemid 44080367)
73. Paavonen J, Naud P, Salmeron J et al. Efficacy of human papillomavirus (HPV)-16/18 AS04-adjuvanted vaccine against cervical infection and precancer caused by oncogenic HPV types (PATRICIA): final analysis of a double-blind, randomised study in young women. Lancet 374(9686), 301-314 (2009).
74. Ault KA. Effect of prophylactic human papillomavirus L1 virus-like-particle vaccine on risk of cervical intraepithelial neoplasia grade 2, grade 3, and adenocarcinoma in situ: a combined analysis of four randomised clinical trials. Lancet 369(9576), 1861-1868 (2007). (Pubitemid 46829356)
75. Munoz N, Kjaer SK, Sigurdsson K et al. Impact of human papillomavirus (HPV)-6/11/16/18 vaccine on all HPV-associated genital diseases in young women. J. Natl Cancer Inst. 102(5), 325-339 (2010).
76. Embers ME, Budgeon LR, Pickel M, Christensen ND. Protective immunity to rabbit oral and cutaneous papillomaviruses by immunization with short peptides of L2, the minor capsid protein. J. Virol. 76(19), 9798-9805 (2002). (Pubitemid 35006520)
77. Gambhira R, Jagu S, Karanam B et al. Protection of rabbits against challenge with rabbit papillomaviruses by immunization with the N terminus of human papillomavirus type 16 minor capsid antigen L2. J. Virol. 81(21), 11585-11592 (2007). (Pubitemid 47623790)
78. Pastrana DV, Gambhira R, Buck CB et al. Cross-neutralization of cutaneous and mucosal Papillomavirus types with anti-sera to the amino terminus of L2. Virology 337(2), 365-372 (2005). (Pubitemid 40803480)
79. Varsani A, Williamson AL, de VD, Becker I, Christensen ND, Rybicki EP. Chimeric human papillomavirus type 16 (HPV-16) L1 particles presenting the common neutralizing epitope for the L2 minor capsid protein of HPV-6 and HPV-16. J. Virol. 77(15), 8386-8393 (2003). (Pubitemid 36871467)
80. Kawana K, Yasugi T, Kanda T et al. Safety and immunogenicity of a peptide containing the cross-neutralization epitope of HPV16 L2 administered nasally in healthy volunteers. Vaccine 21(27-30), 4256-4260 (2003). (Pubitemid 37130271)
81. Roden RB, Yutzy WH, Fallon R, Inglis S, Lowy DR, Schiller JT. Minor capsid protein of human genital papillomaviruses contains subdominant, cross-neutralizing epitopes. Virology 270(2), 254-257 (2000). (Pubitemid 30333671)
82. Kirnbauer R, Taub J, Greenstone H et al. Efficient self-assembly of human papillomavirus type 16 L1 and L1-L2 into virus-like particles. J. Virol. 67(12), 6929-6936 (1993). (Pubitemid 23343814)
83. Slupetzky K, Gambhira R, Culp TD et al. A papillomavirus-like particle (VLP) vaccine displaying HPV16 L2 epitopes induces cross-neutralizing antibodies to HPV11. Vaccine 25(11), 2001-2010 (2007). (Pubitemid 46227679)
84. Pumpens P, Razanskas R, Pushko P et al. Evaluation of HBs, HBc, and frCP virus-like particles for expression of human papillomavirus 16 E7 oncoprotein epitopes. Intervirology 45(1), 24-32 (2002). (Pubitemid 34293699)
85. Kazaks A, Balmaks R, Voronkova T, Ose V, Pumpens P. Melanoma vaccine candidates from chimeric hepatitis B core virus-like particles carrying a tumor-associated MAGE-3 epitope. Biotechnol. J. 3(11), 1429-1436 (2008).
86. Zhang Y, Song S, Liu C et al. Generation of chimeric HBc proteins with epitopes in E.coli: formation of virus-like particles and a potent inducer of antigen-specific cytotoxic immune response and anti-tumor effect in vivo. Cell. Immunol. 247(1), 18-27 (2007). (Pubitemid 47464177)
87. Dorn DC, Lawatscheck R, Zvirbliene A et al. Cellular and humoral immunogenicity of hamster polyomavirus-derived virus-like particles harboring a mucin 1 cytotoxic T-cell epitope. Viral Immunol. 21(1), 12-27 (2008).
88. Pejawar-Gaddy S, Rajawat Y, Hilioti Z et al. Generation of a tumor vaccine candidate based on conjugation of a MUC1 peptide to polyionic papillomavirus virus-like particles. Cancer Immunol. Immunother. 59(11), 1685-1696 (2010).
89. Tegerstedt K, Lindencrona JA, Curcio C et al. A single vaccination with polyomavirus VP1/VP2Her2 virus-like particles prevents outgrowth of HER-2/neu-expressing tumors. Cancer Res. 65(13), 5953-5957 (2005). (Pubitemid 40911202)
90. Andreasson K, Tegerstedt K, Eriksson M et al. Murine pneumotropic virus chimeric Her2/neu virus-like particles as prophylactic and therapeutic vaccines against Her2/neu expressing tumors. Int. J. Cancer 124(1), 150-156 (2009).
91. Eriksson M, Andreasson K, Weidmann J et al. Murine polyomavirus virus-like particles carrying full-length human PSA protect BALB/c mice from outgrowth of a PSA expressing tumor. PLoS One 6(8), e23828 (2011).
92. Braun M, Jandus C, Maurer P et al. Virus-like particles induce robust human T-helper cell responses. Eur. J. Immunol. 42(2), 330-340 (2012).
93. Antimisiaris SG, Kallinteri P, Fatouros DG. Liposomes and Drug Delivery. In: Pharmaceutical Manufacturing Handbook. John Wiley & Sons Inc., Hoboken, NJ USA, 443-533 (2008)
94. Worth LL, Jia SF, An T, Kleinerman ES. ImmTher, a lipophilic disaccharide derivative of muramyl dipeptide, up-regulates specific monocyte cytokine genes and activates monocyte-mediated tumoricidal activity. Cancer Immunol. Immunother. 48(6), 312-320 (1999). (Pubitemid 29434191)
95. Vlad AM, Kettel JC, Alajez NM, Carlos CA, Finn OJ. MUC1 immunobiology: from discovery to clinical applications. Adv. Immunol. 82 82, 249-293 (2004). (Pubitemid 38209513)
96. Sangha R, Butts C. L-BLP25: A peptide vaccine strategy in non-small cell lung cancer. Clin. Cancer Res. 13(15), 4652S-465U3 (2007).
97. Jerome V, Graser A, Muller R, Kontermann RE, Konur A. Cytotoxic T lymphocytes responding to low dose TRP2 antigen are induced against B16 melanoma by liposome-encapsulated TRP2 peptide and CpG DNA adjuvant. J. Immunother. 29(3), 294-305 (2006). (Pubitemid 44297297)
98. Konur A, Graser A, Klam I et al. Liposome-Encapsulated Adjuvants are Potent Inducers of Antigen-Specific T-Cells in Vivo. Open Cancer J. 2, 15-24 (2008).
99. Xiang SD, Scholzen A, Minigo G et al. Pathogen recognition and development of particulate vaccines: Does size matter Methods 40(1), 1-9 (2006). (Pubitemid 44415493)
100. Robson NC, Donachie AM, Mowat AM. Simultaneous presentation and cross-presentation of immune-stimulating complex-associated cognate antigen by antigen-specific B cells. European Journal of Immunology 38(5), 1238-1246 (2008).
101. Morein B, Villacres-Eriksson M, Lovgren-Bengtsson K. Iscom, a delivery system for parenteral and mucosal vaccination. Modulation of the Immune Response to Vaccine Antigens 92, 33-39 (1998).
102. Sjolander S, Drane D, Davis R, Beezum L, Pearse M, Cox J. Intranasal immunisation with influenza-ISCOM induces strong mucosal as well as systemic antibody and cytotoxic T-lymphocyte responses. Vaccine 19(28-29), 4072-4080 (2001). (Pubitemid 32566333)
103. Schnurr M, Orban M, Robson NC et al. ISCOMATRIX Adjuvant Induces Efficient Cross-Presentation of Tumor Antigen by Dendritic Cells via Rapid Cytosolic Antigen Delivery and Processing via Tripeptidyl Peptidase II. J. Immunol. 182(3), 1253-1259 (2009).
104. Davis ID, Chen WS, Jackson H et al. Recombinant NY-ESO-1 protein with ISCOMATRIX adjuvant induces broad integrated antibody and CD4+ and CD8+ T cell responses in humans (vol 101, pg 10697, 2004). Proc. Natl Acad. Sci. USA 102(27), 9734-9734 (2005).
105. Pearse MJ, Drane D. ISCOMATRIX((R)) adjuvant for antigen delivery. Adv. Drug Delivery Rev. 57(3), 465-474 (2005).
106. Krishnan L, Sprott G. Archaeosome adjuvants: Immunological capabilities and mechanism(s) of action. Vaccine 26(17), 2043-2055 (2008).
107. Krishnan L, Sad S, Patel GB, Sprott GD. Archaeosomes induce long-term CD8(+) cytotoxic T cell response to entrapped soluble protein by the exogenous cytosolic pathway, in the absence of CD4(+) T cell help. J. Immunol. 165(9), 5177-5185 (2000).
108. Krishnan L, Sad S, Patel GB, Sprott GD. Archaeosomes induce enhanced cytotoxic T lymphocyte responses to entrapped soluble protein in the absence of interleukin 12 and protect against tumor challenge. Cancer Res. 63(10), 2526-2534 (2003). (Pubitemid 36605193)
109. Krishnan L, nis Sprott G. Archaeosomes as self-adjuvanting delivery systems for cancer vaccines. J. Drug Targeting 11(8-10), 515-524 (2003). (Pubitemid 38519161)
110. Sprott G, Dicaire CJ, Cote JP, Whitfield DM. Adjuvant potential of archaeal synthetic glycolipid mimetics critically depends on the glyco head group structure. Glycobiology 18(7), 559-565 (2008). (Pubitemid 351865836)
111. Kunisawa J, Nakagawa S, Mayumi T. Pharmacotherapy by intracellular delivery of drugs using fusogenic liposomes: application to vaccine development. Adv. Drug Delivery Reviews 52(3), 177-186 (2001). (Pubitemid 33097544)
112. Yoshikawa T, Okada N, Tsujino M et al. Vaccine efficacy of fusogenic liposomes containing tumor cell-lysate against murine B16BL6 melanoma. Biol. Pharma. Bulletin 29(1), 100-104 (2006). (Pubitemid 43036703)
113. Walker C, Selby M, Erickson A, Cataldo D, Valensi JP, VanNest G. Cationic Lipids Direct A Viral Glycoprotein Into the Class-I Major Histocompatibility Complex Antigen-Presentation Pathway. Proc. Natl Acad. Sci. USA 89(17), 7915-7918 (1992).
114. Chen W, Carbone FR, McCluskey J. Electroporation and commercial liposomes efficiently deliver soluble protein into the MHC class I presentation pathway. Priming in vitro and in vivo for class I-restricted recognition of soluble antigen. J. Immunol. Methods 160(1), 49-57 (1993).
115. Chikh G, Schutze-Redelmeir MP. Liposomal delivery of CTL epitopes to dendritic cells. Biosci. Rep. 22(2), 339-353 (2002). (Pubitemid 35222740)
116. Ignatius R, Mahnke K, Rivera M et al. Presentation of proteins encapsulated in sterically stabilized liposomes by dendritic cells initiates CD8(+) T-cell responses in vivo. Blood 96(10), 3505-3513 (2000).
117. Aoki H, Mizuno M, Natsume A et al. Dendritic cells pulsed with tumor extract-cationic liposome complex increase the induction of cytotoxic T lymphocytes in mouse brain tumor. Cancer Immunology Immunotherapy 50(9), 463-468 (2001). (Pubitemid 33079342)
118. Suzuki Y, Wakita D, Chamoto K et al. Liposome-encapsulated CpG oligodeoxynucleotides as a potent adjuvant for inducing type 1 innate immunity. Cancer Res. 64(23), 8754-8760 (2004). (Pubitemid 39552093)
119. Rudginsky S, Siders W, Ingram L, Marshall J, Scheule R, Kaplan J. Antitumor activity of cationic lipid complexed with immunostimulatory DNA. Mol. Ther. 4(4), 347-355 (2001). (Pubitemid 33040520)
120. Gursel I, Gursel M, Ishii KJ, Klinman DM. Sterically stabilized cationic liposomes improve the uptake and immunostimulatory activity of CpG oligonucleotides. J. Immunol. 167(6), 3324-3328 (2001). (Pubitemid 32852574)
121. Cui ZG, Han SJ, Huang L. Coating of mannan on LPD particles containing HPV E7 peptide significantly enhances immunity against HPV-positive tumor. Pharma. Res. 21(6), 1018-1025 (2004). (Pubitemid 38870153)
122. Cui Z, Huang L. Liposome-polycation-DNA (LPD) particle as a carrier and adjuvant for protein-based vaccines: therapeutic effect against cervical cancer. Cancer Immunol. Immunother. 54(12), 1180-1190 (2005). (Pubitemid 41416950)
123. Tan Y, Li S, Pitt BR, Huang L. The inhibitory role of CpG immunostimulatory motifs in cationic lipid vector-mediated transgene expression in vivo. Hum. Gene Ther. 10(13), 2153-2161 (1999). (Pubitemid 29416295)
124. Dileo J, Banerjee R, Whitmore M, Nayak JV, Falo LD, Jr., Huang L. Lipidprotamine-DNA-mediated antigen delivery to antigen-presenting cells results in enhanced anti-tumor immune responses. Mol. Ther. 7(5 Pt 1), 640-648 (2003). (Pubitemid 36626244)
125. Bedikian AY, Del Vecchio M. Allovectin-7 therapy in metastatic melanoma. Expert Opin. Biol. Ther. 8(6), 839-844 (2008). (Pubitemid 351860213)
126. Lv H, Zhang S, Wang B, Cui S, Yan J. Toxicity of cationic lipids and cationic polymers in gene delivery. J. Control. Release 114(1), 100-109 (2006). (Pubitemid 44128621)
127. Sakurai F, Terada T, Yasuda K, Yamashita F, Takakura Y, Hashida M. The role of tissue macrophages in the induction of proinflammatory cytokine production following intravenous injection of lipoplexes. Gene Ther. 9(16), 1120-1126 (2002).
128. Yan W, Chen W, Huang L. Reactive oxygen species play a central role in the activity of cationic liposome based cancer vaccine. J. Control. Release 130(1), 22-28 (2008).
129. Amidi M, Mastrobattista E, Jiskoot W, Hennink WE. Chitosan-based delivery systems for protein therapeutics and antigens. Adv. Drug Delivery Rev. 62(1), 59-82 (2010).
130. Liu Z, Lv D, Liu S et al. Alginic acid-coated chitosan nanoparticles loaded with legumain dna vaccine: effect against breast cancer in mice. PLoS One 8(4), e60190 (2013).
131. Chen H, Li P, Yin Y et al. The promotion of type 1 T helper cell responses to cationic polymers in vivo via toll-like receptor-4 mediated IL-12 secretion. Biomaterials 31(32), 8172-8180 (2010).
132. Huang Z, Yang Y, Jiang Y et al. Anti-tumor immune responses of tumor-associated macrophages via toll-like receptor 4 triggered by cationic polymers. Biomaterials 34(3), 746-755 (2013).
133. De Rosa G, La Rotonda MI, Quaglia F, Ungaro F. Use of additives in the design of poly(lactide-co-glycolide) microspheres for drug delivery. In: Handbook of Particulate Drug Delivery. Kumar R (Eds). American Scientific Publishers, USA, 2008)
134. Hamdy S, Haddadi A, Hung RW, Lavasanifar A. Targeting dendritic cells with nano-particulate PLGA cancer vaccine formulations. Adv. Drug Delivery Rev. 63(10-11), 943-955 (2011).
135. Newman KD, Elamanchili P, Kwon GS, Samuel J. Uptake of poly(D,L-lactic-coglycolic acid) microspheres by antigen-presenting cells in vivo. J. Biomed. Mater. Res. 60(3), 480-486 (2002).
136. Waeckerle-Men Y, Uetz-von Allmen E, Gander B et al. Encapsulation of proteins and peptides into biodegradable poly(D,Llactide-co-glycolide) microspheres prolongs and enhances antigen presentation by human dendritic cells. Vaccine 24(11), 1847-1857 (2006). (Pubitemid 43238266)
137. Johansen P, Gomez JM, Gander B. Development of synthetic biodegradable microparticulate vaccines: a roller coaster story. Expert Rev. Vaccines 6(4), 471-474 (2007). (Pubitemid 47304024)
138. Eldridge JH, Staas JK, Meulbroek JA, Tice TR, Gilley RM. Biodegradable and biocompatible Poly(Dl-Lactide-Co-Glycolide) microspheres as an adjuvant for staphylococcal enterotoxin-B toxoid which enhances the level of toxin-neutralizing antibodies. Infect. Immun. 59(9), 2978-2986 (1991).
139. O'Hagan DT, Jeffery H, Davis SS. Long-term antibody-responses in mice following subcutaneous immunization with ovalbumin entrapped in biodegradable microparticles. Vaccine 11(9), 965-969 (1993). (Pubitemid 23218807)
140. Men Y, Tamber H, Audran R, Gander B, Corradin G. Induction of a cytotoxic T lymphocyte response by immunization with a malaria specific CTL peptide entrapped in biodegradable polymer microspheres. Vaccine 15(12-13), 1405-1412 (1997). (Pubitemid 27397821)
141. Maloy KJ, Donachie AM, Ohagan DT, Mowat AM. Induction of mucosal and systemic immune-responses by immunization with ovalbumin entrapped in poly(Lactide-Co-Glycolide) microparticles. Immunology 81(4), 661-667 (1994). (Pubitemid 24246520)
142. Pinilla-Ibarz J, Cathcart K, Korontsvit T et al. Vaccination of patients with chronic myelogenous leukemia with bcr-abl oncogene breakpoint fusion peptides generates specific immune responses. Blood 95(5), 1781-1787 (2000). (Pubitemid 30120843)
143. Yang YP, Huang CT, Huang XP, Pardoll DM. Persistent Toll-like receptor signals are required for reversal of regulatory T cell-mediated CD8 tolerance. Nat. Immunol. 5(5), 508-515 (2004). (Pubitemid 38660463)
144. Hamdy S, Molavi O, Ma Z et al. Co-delivery of cancer-associated antigen and Toll-like receptor 4 ligand in PLGA nanoparticles induces potent CD8(+) T cell-mediated anti-tumor immunity. Vaccine 26(39), 5046-5057 (2008).
145. Goforth R, Salem AK, Zhu X et al. Immune stimulatory antigen loaded particles combined with depletion of regulatory T-cells induce potent tumor specific immunity in a mouse model of melanoma. Cancer Immunol. Immunother. 58(4), 517-530 (2009).
146. Yoshikawa T, Okada N, Oda A et al. Development of amphiphilic gamma-PGA-nanoparticle based tumor vaccine: Potential of the nanoparticulate cytosolic protein delivery carrier. Biochem. Biophys. Res. Commun. 366(2), 408-413 (2008). (Pubitemid 50010411)
147. Yoshikawa T, Okada N, Oda A et al. Nanoparticles built by self-assembly of amphiphilic gamma-PGA can deliver antigens to antigen-presenting cells with high efficiency: A new tumor-vaccine carrier for eliciting effector T cells. Vaccine 26(10), 1303-1313 (2008).
148. Yamaguchi S, Tatsumi T, Takehara T et al. EphA2-derived peptide vaccine with amphiphilic poly(gamma-glutamic acid) nanoparticles elicits an anti-tumor effect against mouse liver tumor. Cancer Immunol. Immunother. 59(5), 759-767 (2010).
149. Fahmy TM, Demento SL, Caplan MJ, Mellman I, Saltzman WM. Design opportunities for actively targeted nanoparticle vaccines. Nanomedicine (Lond.) 3(3), 343-355 (2008). (Pubitemid 351827311)
150. Silva JM, Videira M, Gaspar R, Preat V, Florindo HF. Immune system targeting by biodegradable nanoparticles for cancer vaccines. J. Control Release.(13), 10-(2013).
151. Hamdy S, Haddadi A, Ghotbi Z, Hung RW, Lavasanifar A. Part I: targeted particles for cancer immunotherapy. Curr. Drug Deliv. 8(3), 261-273 (2011).
152. Heuking S, Iannitelli A, Di SA, Borchard G. Toll-like receptor-2 agonist functionalized biopolymer for mucosal vaccination. Int. J. Pharm. 381(2), 97-105 (2009).
153. Heuking S, Borchard G. Toll-like receptor-7 agonist decoration enhances the adjuvanticity of chitosan-DNA nanoparticles. J. Pharm. Sci. 101(3), 1166-1177 (2012).
154. Heuking S, dam-Malpel S, Sublet E, Iannitelli A, Stefano A, Borchard G. Stimulation of human macrophages (THP-1) using Toll-like receptor-2 (TLR-2) agonist decorated nanocarriers. J. Drug Target 17(8), 662-670 (2009).
155. Faham A, Altin JG. Antigen-containing liposomes engrafted with flagellin-related peptides are effective vaccines that can induce potent antitumor immunity and immunotherapeutic effect. J. Immunol. 185(3), 1744-1754 (2010).
156. Engering A, Geijtenbeek TBH, van Vliet SJ et al. The dendritic cell-specific adhesion receptor DC-SIGN internalizes antigen for presentation to T cells. J. Immunol. 168(5), 2118-2126 (2002). (Pubitemid 34171810)
157. Gazi U, Martinez-Pomares L. Influence of the mannose receptor in host immune responses. Immunobiology 214(7), 554-561 (2009).
158. Irache JM, Salman HH, Gamazo C, Espuelas S. Mannose-targeted systems for the delivery of therapeutics. Expert. Opin. Drug Deliv. 5(6), 703-724 (2008). (Pubitemid 351998259)
159. Opanasopit P, Sakai M, Nishikawa M, Kawakami S, Yamashita F, Hashida M. Inhibition of liver metastasis by targeting of immunomodulators using mannosylated liposome carriers. J. Control. Release. 80(1-3), 283-294 (2002). (Pubitemid 34273766)
160. Kuramoto Y, Kawakami S, Zhou S, Fukuda K, Yamashita F, Hashida M. Use of mannosylated cationic liposomes/immunostimulatory CpG DNA complex for effective inhibition of peritoneal dissemination in mice. J. Gene Med. 10(4), 392-399 (2008). (Pubitemid 351517095)
161. Kuramoto Y, Kawakami S, Zhou S, Fukuda K, Yamashita F, Hashida M. Mannosylated cationic liposomes/CpG DNA complex for the treatment of hepatic metastasis after intravenous administration in mice. J. Pharm. Sci. 98(3), 1193-1197 (2009).
162. Thomann JS, Heurtault B, Weidner S et al. Antitumor activity of liposomal ErbB2/HER2 epitope peptide-based vaccine constructs incorporating TLR agonists and mannose receptor targeting. Biomaterials 32(20), 4574-4583 (2011).
163. Hattori Y, Kawakami S, Lu Y, Nakamura K, Yamashita F, Hashida M. Enhanced DNA vaccine potency by mannosylated lipoplex after intraperitoneal administration. J. Gene Med. 8(7), 824-834 (2006). (Pubitemid 44097138)
164. Hamdy S, Haddadi A, Shayeganpour A, Samuel J, Lavasanifar A. Activation of antigen-specific T cell-responses by mannan-decorated plga nanoparticles. Pharm Res. 28(9), 2288-2301 (2011).
165. Kim TH, Jin H, Kim HW, Cho MH, Cho CS. Mannosylated chitosan nanoparticle-based cytokine gene therapy suppressed cancer growth in BALB/c mice bearing CT-26 carcinoma cells. Mol. Cancer Ther. 5(7), 1723-1732 (2006). (Pubitemid 44323240)
166. Sheng KC, Kalkanidis M, Pouniotis DS et al. Delivery of antigen using a novel mannosylated dendrimer potentiates immunogenicity in vitro and in vivo. Eur. J. Immunol. 38(2), 424-436 (2008).
167. Yu SS, Lau CM, Barham WJ et al. Macrophage-specific RNA interference targeting via "click", mannosylated polymeric micelles. Mol. Pharm. 10(3), 975-987 (2013).
168. Bandyopadhyay A, Fine RL, Demento S, Bockenstedt LK, Fahmy TM. The impact of nanoparticle ligand density on dendritic-cell targeted vaccines. Biomaterials 32(11), 3094-3105 (2011).
169. Joshi MD, Unger WW, van Beelen AJ et al. DC-SIGN mediated antigen-targeting using glycan-modified liposomes: Formulation considerations. Inter. J. Pharmaceutics 416(2), 426-432 (2011).
170. Unger WW, van Beelen AJ, Bruijns SC et al. Glycan-modified liposomes boost CD4+ and CD8+ T-cell responses by targeting DC-SIGN on dendritic cells. J. Control. Release. 160(1), 88-95 (2012).
171. Cruz LJ, Rueda F, Cordobilla B et al. Targeting nanosystems to human DCs via Fc receptor as an effective strategy to deliver antigen for immunotherapy. Mol. Pharm. 8(1), 104-116 (2011).
172. Tacken PJ, Zeelenberg IS, Cruz LJ et al. Targeted delivery of TLR ligands to human and mouse dendritic cells strongly enhances adjuvanticity. Blood 118(26), 6836-6844 (2011).
173. Serre K, Machy P, Grivel JC et al. Efficient presentation of multivalent antigens targeted to various cell surface molecules of dendritic cells and surface Ig of antigen-specific B cells. J. Immunol. 161(11), 6059-6067 (1998). (Pubitemid 28535976)
174. Kawamura K, Kadowaki N, Suzuki R et al. Dendritic cells that endocytosed antigen-containing IgG-liposomes elicit effective antitumor immunity. J. Immunother. 29(2), 165-174 (2006).
175. van Broekhoven CL, Parish CR, Demangel C, Britton WJ, Altin JG. Targeting dendritic cells with antigen-containing liposomes: A highly effective procedure for induction of antitumor immunity and for tumor immunotherapy. Cancer Res. 64(12), 4357-4365 (2004). (Pubitemid 38802444)
176. Castro FV, Tutt AL, White AL et al. CD11c provides an effective immunotarget for the generation of both CD4 and CD8 T cell responses. Eur. J. Immunol. 38(8), 2263-2273 (2008).
177. Wei H, Wang S, Zhang D et al. Targeted delivery of tumor antigens to activated dendritic cells via CD11c molecules induces potent antitumor immunity in mice. Clin. Cancer Res. 15(14), 4612-4621 (2009).
178. Faham A, Altin JG. Ag-bearing liposomes engrafted with peptides that interact with CD11c/CD18 induce potent Ag-specific and antitumor immunity. Int. J. Cancer. 129(6), 1391-1403 (2011).
179. Broos S, Sandin LC, Apel J et al. Synergistic augmentation of CD40-mediated activation of antigen-presenting cells by amphiphilic poly(gamma-glutamic acid) nanoparticles. Biomaterials 33(26), 6230-6239 (2012).
180. Dominguez AL, Lustgarten J. Targeting the tumor microenvironment with anti-neu/anti-CD40 conjugated nanoparticles for the induction of antitumor immune responses. Vaccine 28(5), 1383-1390 (2010).
181. Leleux J, Roy K. Micro and nanoparticle-based delivery systems for vaccine immunotherapy: an immunological and materials perspective. Adv. Healthc. Mater. 2(1), 72-94 (2013).
182. Moghimi SM, Rajabi-Siahboomi R. Advanced colloid-based systems for efficient delivery of drugs and diagnostic agents to the lymphatic tissues. Prog. Biophys. Mol. Biol. 65(3), 221-249 (1996). (Pubitemid 27164027)
183. Oussoren C, Storm G. Lymphatic uptake and biodistribution of liposomes after subcutaneous injection: III. Influence of surface modification with poly (ethyleneglycol). Pharm. Res. 14(10), 1479-1484 (1997). (Pubitemid 27481083)
184. Moghimi SM. The effect of methoxy-PEG chain length and molecular architecture on lymph node targeting of immuno-PEG liposomes. Biomaterials 27(1), 136-144 (2006). (Pubitemid 41225377)
185. Moghimi SM, Moghimi M. Enhanced lymph node retention of subcutaneously injected IgG1-PEG2000-liposomes through pentameric IgM antibody-mediated vesicular aggregation. Biochim. Biophys. Acta. 1778(1), 51-55 (2008).
186. Zhuang Y, Ma Y, Wang C et al. PEGylated cationic liposomes robustly augment vaccine-induced immune responses: Role of lymphatic trafficking and biodistribution. J. Control. Release. 159(1), 135-142 (2012).
187. Owens DE 3rd, Peppas NA. Opsonization, biodistribution, and pharmacokinetics of polymeric nanoparticles. Int. J. Pharm. 307(1), 93-102 (2006). (Pubitemid 41773257)
188. Alexis F, Pridgen E, Molnar LK, Farokhzad OC. Factors affecting the clearance and biodistribution of polymeric nanoparticles. Mol. Pharm. 5(4), 505-515 (2008).
189. Devriendt B, De Geest BG, Goddeeris BM, Cox E. Crossing the barrier: Targeting epithelial receptors for enhanced oral vaccine delivery. J. Control. Release. 160(3), 431-439 (2012).
190. Wilkhu J, McNeil SE, Kirby DJ, Perrie Y. Formulation design considerations for oral vaccines. Ther. Deliv. 2(9), 1141-1164 (2011).
191. Chadwick S, Kriegel C, Amiji M. Nanotechnology solutions for mucosal immunization. Adv. Drug Deliv. Rev. 62(4-5), 394-407 (2010).
192. Zhu Q, Talton J, Zhang G et al. Large intestine-targeted, nanoparticle-releasing oral vaccine to control genitorectal viral infection. Nat. Med. 18(8), 1291-1296 (2012).
193. Lai SK, Wang YY, Hanes J. Mucus-penetrating nanoparticles for drug and gene delivery to mucosal tissues. Adv. Drug Deliv. Rev. 61(2), 158-171 (2009).
194. Torchilin V. Multifunctional and stimuli-sensitive pharmaceutical nanocarriers. Eur. J. Pharm. Biopharm. 71(3), 431-444 (2009).
195. Nembrini C, Stano A, Dane KY et al. Nanoparticle conjugation of antigen enhances cytotoxic T-cell responses in pulmonary vaccination. Proc. Natl Acad.Sci. USA. 108(44), E989-E997 (2011).
196. Ungaro F, d'Angelo I, Miro A, La Rotonda MI, Quaglia F. Engineered PLGA nano-and micro-carriers for pulmonary delivery: challenges and promises. J. Pharm. Pharmacol. 64(9), 1217-1235 (2012).
197. Zhang Z, Tsai PC, Ramezanli T, Michniak-Kohn BB. Polymeric nanoparticles-based topical delivery systems for the treatment of dermatological diseases. Wiley.Interdiscip. Rev. Nanomed. Nanobiotechnol. 5(3), 205-218 (2013).
198. Chen D, Maa YF, Haynes JR. Needle-free epidermal powder immunization. Expert Rev. Vaccines 1(3), 265-276 (2002). (Pubitemid 36559863)
199. Rakhmilevich AL, Imboden M, Hao Z et al. Effective particle-mediated vaccination against mouse melanoma by coadministration of plasmid DNA encoding Gp100 and granulocyte-macrophage colonystimulating factor. Clin. Cancer Res. 7(4), 952-961 (2001). (Pubitemid 32708734)
200. Cassaday RD, Sondel PM, King DM et al. A phase I study of immunization using particle-mediated epidermal delivery of genes for gp100 and GM-CSF into uninvolved skin of melanoma patients. Clin. Cancer Res. 13(2 Pt 1), 540-549 (2007). (Pubitemid 46225360)
201. Buonaguro L, Pulendran B. Immunogenomics and systems biology of vaccines. Immunol. Rev. 239(1), 197-208 (2011).
202. Cruz LJ, Tacken PJ, Fokkink R et al. Targeted PLGA nano-but not microparticles specifically deliver antigen to human dendritic cells via DC-SIGN in vitro. J. Control. Release. 144(2), 118-126 (2010).
203. Hu Y, Litwin T, Nagaraja AR et al. Cytosolic delivery of membrane-impermeable molecules in dendritic cells using pH-responsive coreshell nanoparticles. Nano. Lett. 7(10), 3056-3064 (2007). (Pubitemid 350132930)
204. Faham A, Bennett D, Altin JG. Liposomal Ag engrafted with peptides of sequence derived from HMGB1 induce potent Ag-specific and anti-tumour immunity. Vaccine 27(42), 5846-5854 (2009).