Antigen delivery by virus-like particles for immunotherapeutic vaccination

Therapeutic Delivery

Volumn 5, Issue 11, 2014, Pages 1223-1240

  Al Barwani, Farah ^a,b   Donaldson, Braeden ^a,b   Pelham, Simon J ^b   Young, Sarah L ^b   Ward, Vernon K ^a  

^a UNIVERSITY OF OTAGO   (New Zealand)

^b UNIVERSITY OF OTAGO   (New Zealand)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIGEN; IMMUNOLOGICAL ADJUVANT; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; SUBUNIT VACCINE; VIRUS LIKE PARTICLE VACCINE; EPITOPE;

ADDICTION; ALLERGY; AUTOIMMUNE DISEASE; CANCER IMMUNOTHERAPY; CELLULAR IMMUNITY; CROSS PRESENTATION; HUMAN; HUMORAL IMMUNITY; IMMUNOGENICITY; IMMUNOSTIMULATION; IMMUNOTHERAPY; NEOPLASM; NONHUMAN; PHASE 1 CLINICAL TRIAL (TOPIC); PHASE 2 CLINICAL TRIAL (TOPIC); PHASE 3 CLINICAL TRIAL (TOPIC); REVIEW; VACCINATION; VIRUS IMMUNITY; VIRUS LIKE AGENT; ANIMAL; CHEMISTRY; GENETICS; IMMUNOLOGY; MEDICINAL CHEMISTRY; PHARMACEUTICS; PROCEDURES;

ADJUVANTS, IMMUNOLOGIC; ANIMALS; ANTIGENS; CHEMISTRY, PHARMACEUTICAL; EPITOPES; HUMANS; IMMUNITY, CELLULAR; IMMUNITY, HUMORAL; TECHNOLOGY, PHARMACEUTICAL; VACCINATION; VACCINES, VIRUS-LIKE PARTICLE;

EID: 84917671708     PISSN: 20415990     EISSN: 20416008     Source Type: Journal    
DOI: 10.4155/tde.14.74     Document Type: Review

References (84)

1. Bayer ME, Blumberg BS, Werner B. Particles associated with Australia antigen in the sera of patients with leukaemia, Down's Syndrome and hepatitis. Nature 218(5146), 1057-1059 (1968).
2. Baumert TF, Ito S, Wong DT, Liang TJ. Hepatitis C virus structural proteins assemble into viruslike particles in insect cells. J. Virol. 72(5), 3827-3836 (1998).
3. Green KY, Lew JF, Jiang X, Kapikian AZ, Estes MK. Comparison of the reactivities of baculovirus-expressed recombinant Norwalk virus capsid antigen with those of the native Norwalk virus antigen in serologic assays and some epidemiologic observations. J. Clin. Microbiol. 31(8), 2185-2191 (1993).
4. Donaldson B, Al-Barwani F, Young V, Scullion S, Ward VK, Young SL. Virus-like particles, a versatile subunit vaccine platform. In: Advances in Delivery Science and Technology: Subunit Vaccine Delivery. Foged C, Rades T, Perrie Y and Hook S (Eds.). Springer (2014) (In Press).
5. Shank-Retzlaff ML, Zhao Q, Anderson C et al. Evaluation of the thermal stability of Gardasil. Hum. Vaccin. 2(4), 147-154 (2006).
6. Pincus S, Boddapati S, Li J, Sadowski T. Release and stability testing programs for a novel virus-like particle vaccine. BioPharm Int. 2010, 26-34 (2010).
7. Le Tallec D, Doucet D, Elouahabi A, Harvengt P, Deschuyteneer M, Deschamps M. Cervarix, the GSK HPV-16/HPV-18 AS04-adjuvanted cervical cancer vaccine, demonstrates stability upon long-term storage and under simulated cold chain break conditions. Hum. Vaccin. 5(7), 467-474 (2009).
8. Keating GM, Noble S. Recombinant hepatitis B vaccine (Engerix-B): a review of its immunogenicity and protective efficacy against hepatitis B. Drugs 63(10), 1021-1051 (2003).
9. Crawford SE, Labbe M, Cohen J, Burroughs MH, Zhou YJ, Estes MK. Characterization of virus-like particles produced by the expression of rotavirus capsid proteins in insect cells. J. Virol. 68(9), 5945-5952 (1994).
10. Sabara M, Parker M, Aha P et al. Assembly of doubleshelled rotaviruslike particles by simultaneous expression of recombinant VP6 and VP7 proteins. J. Virol. 65(12), 6994-6997 (1991).
11. Latham T, Galarza JM. Formation of wild-type and chimeric influenza virus-like particles following simultaneous expression of only four structural proteins. J. Virol. 75(13), 6154-6165 (2001).
12. Wiedermann U, Wiltschke C, Jasinska J et al. A virosomal formulated Her-2/neu multi-peptide vaccine induces Her-2/neu-specific immune responses in patients with metastatic breast cancer: a Phase I study. Breast Cancer Res. Treat. 119(3), 673-683 (2010).
13. Peacey M, Wilson S, Baird MA, Ward VK. Versatile RHDV virus-like particles: incorporation of antigens by genetic modification and chemical conjugation. Biotechnol. Bioeng. 98(5), 968-977 (2007).
14. 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).
15. Lasickiene R, Gedvilaite A, Norkiene M et al. The use of recombinant pseudotype virus-like particles harbouring inserted target antigen to generate antibodies against cellular marker p16INK4A. ScientificWorldJournal 2012, 263737 (2012).
16. Mazeike E, Gedvilaite A, Blohm U. Induction of insertspecific immune response in mice by hamster polyomavirus VP1 derived virus-like particles carrying LCMV GP33 CTL epitope. Virus Res. 163(1), 2-10 (2012).
17. Middelberg AP, Rivera-Hernandez T, Wibowo N et al. A microbial platform for rapid and low-cost virus-like particle and capsomere vaccines. Vaccine 29(41), 7154-7162 (2011).
18. 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).
19. Gregson AL, Oliveira G, Othoro C et al. Phase I trial of an alhydrogel adjuvanted hepatitis B core virus-like particle containing epitopes of Plasmodium falciparum circumsporozoite protein. PLoS ONE 3(2), e1556 (2008).
20. Fiers W, De Filette M, El Bakkouri K et al. M2e-based universal influenza A vaccine. Vaccine 27(45), 6280-6283 (2009).
21. Yusibov V, Hooper DC, Spitsin SV et al. Expression in plants and immunogenicity of plant virus-based experimental rabies vaccine. Vaccine 20(25-26), 3155-3164 (2002).
22. 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).
23. Li K, Peers-Adams A, Win SJ et al. Antigen incorporated in virus-like particles is delivered to specific dendritic cell subsets that induce an effective antitumor immune response in vivo. J. Immunother. 36(1), 11-19 (2013).
24. McKee SJ, Young VL, Clow F et al. Virus-like particles and alpha-galactosylceramide form a self-adjuvanting composite particle that elicits anti-tumor responses. J. Control. Release 159(3), 338-345 (2012).
25. Smith MT, Hawes AK, Bundy BC. Reengineering viruses and virus-like particles through chemical functionalization strategies. Curr. Opin. Biotechnol. 24.4, 620-626 (2013).
26. Patel KG, Swartz JR. Surface functionalization of viruslike particles by direct conjugation using azide-alkyne click chemistry. Bioconjug. Chem. 22(3), 376-387 (2011).
27. Chackerian B, Durfee MR, Schiller JT. Virus-like display of a neo-self antigen reverses B cell anergy in a B cell receptor transgenic mouse model. J. Immunol. 180(9), 5816-5825 (2008).
28. Win SJ, McMillan DG, Errington-Mais F et al. Enhancing the immunogenicity of tumour lysate-loaded dendritic cell vaccines by conjugation to virus-like particles. Br. J. Cancer 106(1), 92-98 (2012).
29. Zeltins A. Construction and characterization of virus-like particles: a review. Mol. Biotechnol. 53(1), 92-107 (2013).
30. Fang CY, Lin PY, Ou WC et al. Analysis of the size of DNA packaged by the human JC virus-like particle. J. Virol. Methods 182(1-2), 87-92 (2012).
31. Ou WC, Wang M, Fung CY et al. The major capsid protein, VP1, of human JC virus expressed in Escherichia coli is able to self-assemble into a capsid-like particle and deliver exogenous DNA into human kidney cells. J. Gen. Virol. 80 (Pt 1), 39-46 (1999).
32. Chen LS, Wang M, Ou WC et al. Efficient gene transfer using the human JC virus-like particle that inhibits human colon adenocarcinoma growth in a nude mouse model. Gene Ther. 17(8), 1033-1041 (2010).
33. El Mehdaoui S, Touze A, Laurent S, Sizaret PY, Rasschaert D, Coursaget P. Gene transfer using recombinant rabbit hemorrhagic disease virus capsids with genetically modified DNA encapsidation capacity by addition of packaging sequences from the L1 or L2 protein of human papillomavirus type 16. J. Virol. 74(22), 10332-10340 (2000).
34. Pichlmair A, Habjan M, Unger H, Weber F. Virus-like particles expressing the nucleocapsid gene as an efficient vaccine against Rift Valley fever virus. Vector Borne Zoonotic Dis. 10(7), 701-703 (2010).
35. Lu X, Thompson JR, Perry KL. Encapsidation of DNA, a protein and a fluorophore into virus-like particles by the capsid protein of cucumber mosaic virus. J. Gen. Virol. 93(Pt 5), 1120-1126 (2012).
36. Boudreaux C, Vile D, Gilmore B, Tanner J, Kelly D, McDonald S. Rotavirus core shell subdomains involved in polymerase encapsidation into virus-like particles. J. Gen. Virol. 94(8), 1818-1826 (2013).
37. Fiedler JD, Brown SD, Lau JL, Finn MG. RNA-directed packaging of enzymes within virus-like particles. Angew Chem. Int. Ed. Engl. 49(50), 9648-9651 (2010).
38. Minten IJ, Hendriks LJ, Nolte RJ, Cornelissen JJ. Controlled encapsulation of multiple proteins in virus capsids. J. Am. Chem. Soc. 131(49), 17771-17773 (2009).
39. Hunter Z, Smyth HD, Durfee P, Chackerian B. Induction of mucosal and systemic antibody responses against the HIV coreceptor CCR5 upon intramuscular immunization and aerosol delivery of a virus-like particle based vaccine. Vaccine 28(2), 403-414 (2009).
40. El-Kamary SS, Pasetti MF, Mendelman PM et al. Adjuvanted intranasal Norwalk virus-like particle vaccine elicits antibodies and antibody-secreting cells that express homing receptors for mucosal and peripheral lymphoid tissues. J. Infect. Dis. 202(11), 1649-1658 (2010).
41. Paolicelli P, Prego C, Sanchez A, Alonso MJ. Surfacemodified PLGA-based nanoparticles that can efficiently associate and deliver virus-like particles. Nanomedicine (Lond.) 5(6), 843-853 (2010).
42. 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 5(10), e13460 (2010).
43. Biemelt S, Sonnewald U, Galmbacher P, Willmitzer L, Muller M. Production of human papillomavirus type 16 virus-like particles in transgenic plants. J. Virol. 77(17), 9211-9220 (2003).
44. Jegerlehner A, Tissot A, Lechner F et al. A molecular assembly system that renders antigens of choice highly repetitive for induction of protective B cell responses. Vaccine 20(25-26), 3104-3112 (2002).
45. 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).
46. Win SJ, Ward VK, Dunbar PR, Young SL, Baird MA. Cross-presentation of epitopes on virus-like particles via the MHC I receptor recycling pathway. Immunol. Cell Biol. 89(6), 681-688 (2011).
47. McIntosh JD, Manning K, Chokshi S et al. An engineered non-toxic superantigen increases cross presentation of hepatitis B virus nucleocapsids by human dendritic cells. PLoS ONE 9(4), e93598 (2014).
48. Romanowski B. Long term protection against cervical infection with the human papillomavirus: review of currently available vaccines. Hum. Vaccin. 7(2), 161-169 (2011).
49. Lopez-Macias C, Ferat-Osorio E, Tenorio-Calvo A et al. Safety and immunogenicity of a virus-like particle pandemic influenza A (H1N1) 2009 vaccine in a blinded, randomized, placebo-controlled trial of adults in Mexico. Vaccine 29(44), 7826-7834 (2011).
50. Link A, Zabel F, Schnetzler Y, Titz A, Brombacher F, Bachmann MF. Innate immunity mediates follicular transport of particulate but not soluble protein antigen. J. Immunol. 188(8), 3724-3733 (2012).
51. Bessa J, Zabel F, Link A et al. Low-affinity B cells transport viral particles from the lung to the spleen to initiate antibody responses. Proc. Natl Acad. Sci. USA 109(50), 20566-20571 (2012).
52. Basha G, Omilusik K, Chavez-Steenbock A et al. A CD74- dependent MHC class I endolysosomal cross-presentation pathway. Nat. Immunol. 13(3), 237-245 (2012).
53. Joffre OP, Segura E, Savina A, Amigorena S. Crosspresentation by dendritic cells. Nat. Rev. Immunol. 12(8), 557-569 (2012).
54. Keller SA, von Allmen CE, Hinton HJ et al. Follicular and marginal zone B cells fail to cross-present MHC class I-restricted epitopes derived from viral particles. J. Immunol. 182(10), 6261-6266 (2009).
55. Speiser DE, Schwarz K, Baumgaertner P et al. Memory and effector CD8 T-cell responses after nanoparticle vaccination of melanoma patients. J. Immunother. 33(8), 848-858 (2010).
56. Jegerlehner A, Maurer P, Bessa J, Hinton HJ, Kopf M, Bachmann MF. TLR9 signaling in B cells determines class switch recombination to IgG2a. J. Immunol. 178(4), 2415-2420 (2007).
57. 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).
58. Skountzou I, Quan FS, Gangadhara S et al. Incorporation of glycosylphosphatidylinositol-anchored granulocytemacrophage colony-stimulating factor or CD40 ligand enhances immunogenicity of chimeric simian immunodeficiency virus-like particles. J. Virol. 81(3), 1083-1094 (2007).
59. Dunn GP, Bruce AT, Ikeda H, Old LJ, Schreiber RD. Cancer immunoediting: from immunosurveillance to tumor escape. Nat. Immunol. 3(11), 991-998 (2002).
60. Jemon K, Young V, Wilson M et al. An enhanced heterologous virus-like particle for human papillomavirus type 16 tumour immunotherapy. PLoS ONE 8(6), e66866 (2013).
61. Zhang S, Yong LK, Li D, Cubas R, Chen C, Yao Q. Mesothelin virus-like particle immunization controls pancreatic cancer growth through CD8+ T cell induction and reduction in the frequency of CD4+ foxp3+ ICOSregulatory T cells. PLoS ONE 8(7), e68303 (2013).
62. Martin Caballero J, Garzon A, Gonzalez-Cintado L et al. Chimeric infectious bursal disease virus-like particles as potent vaccines for eradication of established HPV-16 E7- dependent tumors. PLoS ONE 7(12), e52976 (2012).
63. Present DH, Rutgeerts P, Targan S et al. Infliximab for the treatment of fistulas in patients with Crohn's disease. N. Engl. J. Med. 340(18), 1398-1405 (1999).
64. Danese S, Colombel JF, Peyrin-Biroulet L, Rutgeerts P, Reinisch W. Review article: the role of anti-TNF in the management of ulcerative colitis -past, present and future. Aliment. Pharmacol. Ther. 37(9), 855-866 (2013).
65. Jirasiritham S, Sumethkul V, Mavichak V, Lertsithichai P, Jirasiritham S. The role of anti-IL-2 receptor in highrisk kidney transplant patients. Transplant. Proc. 36(7), 2110-2112 (2004).
66. Spohn G, Keller I, Beck M, Grest P, Jennings GT, Bachmann MF. Active immunization with IL-1 displayed on viruslike particles protects from autoimmune arthritis. Eur. J. Immunol. 38(3), 877-887 (2008).
67. Rohn TA, Jennings GT, Hernandez M et al. Vaccination against IL-17 suppresses autoimmune arthritis and encephalomyelitis. Eur. J. Immunol. 36(11), 2857-2867 (2006).
68. 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).
69. Tang Y, Luo X, Cui H et al. MicroRNA-146A contributes to abnormal activation of the type I interferon pathway in human lupus by targeting the key signaling proteins. Arthritis Rheum. 60(4), 1065-1075 (2009).
70. Pan Y, Jia T, Zhang Y et al. MS2 VLP-based delivery of microRNA-146a inhibits autoantibody production in lupus-prone mice. Int. J. Nanomedicine 7, 5957-5967 (2012).
71. Winther L, Arnved J, Malling HJ, Nolte H, Mosbech H. Side-effects of allergen-specific immunotherapy: a prospective multi-centre study. Clin. Exp. Allergy 36(3), 254-260 (2006).
72. Klimek L, Willers J, Hammann-Haenni A et al. Assessment of clinical efficacy of CYT003-QbG10 in patients with allergic rhinoconjunctivitis: a Phase IIb study. Clin. Exp. Allergy 41(9), 1305-1312 (2011).
73. Beeh KM, Kanniess F, Wagner F et al. The novel TLR-9 agonist QbG10 shows clinical efficacy in persistent allergic asthma. J. Allergy Clin. Immunol. 131(3), 866-874 (2013).
74. WHO. Global Brief on Hypertension. World Health Organisation (2013).
75. Matchar DB, McCrory DC, Orlando LA et al. Systematic review: comparative effectiveness of angiotensin-converting enzyme inhibitors and angiotensin II receptor blockers for treating essential hypertension. Ann. Intern. Med. 148(1), 16-29 (2008).
76. Maurer P, Bachmann MF. Immunization against angiotensins for the treatment of hypertension. Clin. Immunol. 134(1), 89-95 (2010).
77. Orgogozo JM, Gilman S, Dartigues JF et al. Subacute meningoencephalitis in a subset of patients with AD after Abeta42 immunization. Neurology 61(1), 46-54 (2003).
78. Chackerian B, Rangel M, Hunter Z, Peabody DS. Virus and virus-like particle-based immunogens for Alzheimer's disease induce antibody responses against amyloid-beta without concomitant T cell responses. Vaccine 24(37-39), 6321-6331 (2006).
79. Zamora E, Handisurya A, Shafti-Keramat S et al. Papillomavirus-like particles are an effective platform for amyloid-beta immunization in rabbits and transgenic mice. J. Immunol. 177(4), 2662-2670 (2006).
80. Maurer P, Jennings GT, Willers J et al. A therapeutic vaccine for nicotine dependence: preclinical efficacy, and Phase I safety and immunogenicity. Eur. J. Immunol. 35(7), 2031-2040 (2005).
81. Cornuz J, Zwahlen S, Jungi WF et al. A vaccine against nicotine for smoking cessation: a randomized controlled trial. PLoS ONE 3(6), e2547 (2008).
82. Groothuis TA, Neefjes J. The many roads to crosspresentation. J. Exp. Med. 202(10), 1313-1318 (2005).
83. Lee YN, Lee YT, Kim MC et al. Fc receptor is not required for inducing antibodies but plays a critical role in conferring protection after influenza M2 vaccination. Immunology 143(2), 300-309 (2014).
84. Landry N, Ward BJ, Trepanier S et al. Preclinical and clinical development of plant-made virus-like particle vaccine against avian H5N1 influenza. PLoS ONE 5(12), e15559 (2010).