Nanoformulation of synergistic TLR ligands to enhance vaccination against Entamoeba histolytica

Vaccine

Volumn 35, Issue 6, 2017, Pages 916-922

  Abhyankar, Mayuresh M ^a   Noor, Zannatun ^a   Tomai, Mark A ^b   Elvecrog, James ^b   Fox, Christopher B ^c,d   Petri, William A ^a  

^a UNIVERSITY OF VIRGINIA   (United States)

^b 3M COMPANY   (United States)

^c IDRI   (United States)

^d UNIVERSITY OF WASHINGTON   (United States)

Author keywords

Amebiasis; Entamoeba; Immune response; Liposome; Vaccine

Indexed keywords

3M 052; AMEBIASIS VACCINE; EM 014; GAMMA INTERFERON; IMMUNOGLOBULIN A; IMMUNOGLOBULIN G1; IMMUNOGLOBULIN G2A; IMMUNOLOGICAL ADJUVANT; INTERLEUKIN 17; INTERLEUKIN 2; INTERLEUKIN 4; LECA ANTIGEN; PARASITE ANTIGEN; RETINOIC ACID; TOLL LIKE RECEPTOR 4; TOLL LIKE RECEPTOR 7; TOLL LIKE RECEPTOR 8; TOLL LIKE RECEPTOR AGONIST; UNCLASSIFIED DRUG; ALUMINUM POTASSIUM SULFATE; ALUMINUM SULFATE; LECTIN; LIPOPOLYSACCHARIDE; LIPOSOME; MEMBRANE PROTEIN; MF59 OIL EMULSION; OLIGODEOXYRIBONUCLEOTIDE; POLYSORBATE; PROTOZOAL VACCINE; PROTOZOON ANTIBODY; RNA; SQUALENE; SUBUNIT VACCINE; TLR3 PROTEIN, MOUSE; TLR7 PROTEIN, MOUSE; TLR8 PROTEIN, MOUSE; TOLL LIKE RECEPTOR 3;

ADJUVANT THERAPY; AMEBIASIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIBODY TITER; ANTIGEN DETECTION; ARTICLE; CELLULAR IMMUNITY; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RESPONSE; DRUG DELIVERY SYSTEM; DRUG FORMULATION; DRUG POTENTIATION; EMULSION; ENTAMOEBA HISTOLYTICA; FEMALE; HUMORAL IMMUNITY; IMMUNE RESPONSE; IMMUNIZATION; IMMUNOGENICITY; IN VITRO STUDY; MAMMAL CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; TH1 CELL; AGONISTS; ANIMAL; BIOSYNTHESIS; CBA MOUSE; CHEMISTRY; DRUG EFFECTS; GENETICS; GROWTH, DEVELOPMENT AND AGING; IMMUNOLOGY; MUCOSAL IMMUNITY; PARASITOLOGY;

ADJUVANTS, IMMUNOLOGIC; ALUM COMPOUNDS; ANIMALS; ANTIBODIES, PROTOZOAN; ANTIGENS, PROTOZOAN; ENTAMOEBA HISTOLYTICA; ENTAMOEBIASIS; IMMUNITY, MUCOSAL; IMMUNIZATION; INTERFERON-GAMMA; INTERLEUKIN-17; LECTINS; LIPOPOLYSACCHARIDES; LIPOSOMES; MEMBRANE GLYCOPROTEINS; MICE; MICE, INBRED CBA; OLIGODEOXYRIBONUCLEOTIDES; POLYSORBATES; PROTOZOAN VACCINES; RNA; SQUALENE; TOLL-LIKE RECEPTOR 3; TOLL-LIKE RECEPTOR 7; TOLL-LIKE RECEPTOR 8; TRETINOIN; VACCINES, SUBUNIT;

EID: 85009517437     PISSN: 0264410X     EISSN: 18732518     Source Type: Journal    
DOI: 10.1016/j.vaccine.2016.12.057     Document Type: Article

References (48)

1. [1] WHO. WHO fact sheet N0 330. Diarrheal disease. WHO; 2013.
2. [2] Moore, S.R., Lima, A.A., Conaway, M.R., Schorling, J.B., Soares, A.M., Guerrant, R.L., Early childhood diarrhoea and helminthiases associate with long-term linear growth faltering. Int J Epidemiol 30:6 (2001), 1457–1464.
3. [3] Petri, W.A., Miller, M., Binder, H.J., Levine, M.M., Dillingham, R., Guerrant, R.L., Enteric infections, diarrhea, and their impact on function and development. J Clin Invest 118:4 (2008), 1277–1290.
4. [4] Ansong, D., Asante, K.P., Vekemans, J., Owusu, S.K., Owusu, R., Brobby, N.A.W., et al. T cell responses to the RTS, S/AS01(E) and RTS, S/AS02(D) malaria candidate vaccines administered according to different schedules to Ghanaian children. PLoS ONE, 6(4), 2011, e18891.
5. [5] Schwendener, R.A., Liposomes as vaccine delivery systems: a review of the recent advances. Ther Adv Vacc 2:6 (2014), 159–182.
6. [6] Fox, C.B., Sivananthan, S.J., Duthie, M.S., Vergara, J., Guderian, J.A., Moon, E., et al. A nanoliposome delivery system to synergistically trigger TLR4 AND TLR7. J Nanobiotechnol, 26(12), 2014, 17.
7. [7] O'Hagan, D.T., Fox, C.B., New generation adjuvants–from empiricism to rational design. Vaccine 8:33 Suppl 2 (2015), B14–B20.
8. [8] Zhang, W.-W., Matlashewski, G., Immunization with a Toll-like receptor 7 and/or 8 agonist vaccine adjuvant increases protective immunity against Leishmania major in BALB/c mice. Infect Immun 76:8 (2008), 3777–3783.
9. [9] Kotloff, K.L., Nataro, J.P., Blackwelder, W.C., Nasrin, D., Farag, T.H., Panchalingam, S., et al. Burden and aetiology of diarrhoeal disease in infants and young children in developing countries (the Global Enteric Multicenter Study, GEMS): a prospective, case-control study. Lancet Lond Engl 382:9888 (2013), 209–222.
10. [10] Mondal, D., Petri, W.A., Sack, R.B., Kirkpatrick, B.D., Haque, R., Entamoeba histolytica-associated diarrheal illness is negatively associated with the growth of preschool children: evidence from a prospective study. Trans R Soc Trop Med Hyg 100:11 (2006), 1032–1038.
11. [11] Quach, J., St-Pierre, J., Chadee, K., The future for vaccine development against Entamoeba histolytica. Hum Vacc Immunother 10:6 (2014), 1514–1521.
12. [12] Roncolato, E.C., Teixeira, J.E., Barbosa, J.E., Zambelli Ramalho, L.N., Huston, C.D., Immunization with the Entamoeba histolytica surface metalloprotease EhMSP-1 protects hamsters from amebic liver abscess. Infect Immun 83:2 (2015), 713–720.
13. [13] Barroso, L., Abhyankar, M., Noor, Z., Read, K., Pedersen, K., White, R., et al. Expression, purification, and evaluation of recombinant LecA as a candidate for an amebic colitis vaccine. Vaccine 32:10 (2014), 1218–1224.
14. [14] Matzinger, P., Tolerance, danger, and the extended family. Annu Rev Immunol 12 (1994), 991–1045.
15. [15] Moser, M., Leo, O., Key concepts in immunology. Vaccine 28:Suppl 3 (2010), C2–C13.
16. [16] Haque, R., Ali, I.M., Sack, R.B., Farr, B.M., Ramakrishnan, G., Petri, W.A., Amebiasis and mucosal IgA antibody against the Entamoeba histolytica adherence lectin in Bangladeshi children. J Infect Dis 183:12 (2001), 1787–1793.
17. [17] Haque, R., Mondal, D., Shu, J., Roy, S., Kabir, M., Davis, A.N., et al. Correlation of interferon-gamma production by peripheral blood mononuclear cells with childhood malnutrition and susceptibility to amebiasis. Am J Trop Med Hyg 76:2 (2007), 340–344.
18. [18] Guo, X., Barroso, L., Becker, S.M., Lyerly, D.M., Vedvick, T.S., Reed, S.G., et al. Protection against intestinal amebiasis by a recombinant vaccine is transferable by T cells and mediated by gamma interferon. Infect Immun 77:9 (2009), 3909–3918.
19. [19] Houpt, E., Barroso, L., Lockhart, L., Wright, R., Cramer, C., Lyerly, D., et al. Prevention of intestinal amebiasis by vaccination with the Entamoeba histolytica Gal/GalNac lectin. Vaccine 22:5–6 (2004), 611–617.
20. [20] Fox, C.B., Moutaftsi, M., Vergara, J., Desbien, A.L., Nana, G.I., Vedvick, T.S., et al. TLR4 ligand formulation causes distinct effects on antigen-specific cell-mediated and humoral immune responses. Vaccine 31:49 (2013), 5848–5855.
21. [21] Fox, C.B., Characterization of TLR4 agonist effects on alhydrogel® sedimentation: a novel application of laser scattering optical profiling. J Pharm Sci 101:11 (2012), 4357–4364.
22. [22] Misquith, A., Fung, H.W.M., Dowling, Q.M., Guderian, J.A., Vedvick, T.S., Fox, C.B., In vitro evaluation of TLR4 agonist activity: formulation effects. Colloids Surf B Biointerfaces 1:113 (2014), 312–319.
23. [23] Smirnov, D., Schmidt, J.J., Capecchi, J.T., Wightman, P.D., Vaccine adjuvant activity of 3M–052: an imidazoquinoline designed for local activity without systemic cytokine induction. Vaccine 29:33 (2011), 5434–5442.
24. [24] Diamond, L.S., Harlow, D.R., Cunnick, C.C., A new medium for the axenic cultivation of Entamoeba histolytica and other Entamoeba. Trans R Soc Trop Med Hyg 72:4 (1978), 431–432.
25. [25] Soong, C.J., Kain, K.C., Abd-Alla, M., Jackson, T.F., Ravdin, J.I., A recombinant cysteine-rich section of the Entamoeba histolytica galactose-inhibitable lectin is efficacious as a subunit vaccine in the gerbil model of amebic liver abscess. J Infect Dis 171:3 (1995), 645–651.
26. [26] Ravdin, J.I., Guerrant, R.L., Role of adherence in cytopathogenic mechanisms of Entamoeba histolytica. Study with mammalian tissue culture cells and human erythrocytes. J Clin Invest 68:5 (1981), 1305–1313.
27. [27] Jin, W., Dong, C., IL-17 cytokines in immunity and inflammation. Emerg Microbes Infect, 2(9), 2013, e60.
28. [28] Thakur, A., Pedersen, L.E., Jungersen, G., Immune markers and correlates of protection for vaccine induced immune responses. Vaccine 30:33 (2012), 4907–4920.
29. + T cell- and IL-17-mediated protection against Entamoeba histolytica induced by a recombinant vaccine. Vaccine 29:4 (2011), 772–777.
30. [30] Hammerschmidt, S.I., Friedrichsen, M., Boelter, J., Lyszkiewicz, M., Kremmer, E., Pabst, O., et al. Retinoic acid induces homing of protective T and B cells to the gut after subcutaneous immunization in mice. J Clin Invest 121:8 (2011), 3051–3061.
31. [31] Tan, X., Sande, J.L., Pufnock, J.S., Blattman, J.N., Greenberg, P.D., Retinoic acid as a vaccine adjuvant enhances CD8+ T cell response and mucosal protection from viral challenge. J Virol 85:16 (2011), 8316–8327.
32. [32] Fox, C.B., Carter, D., Kramer, R.M., Beckmann, A.M., Reed, S.G., Current status of TLR4 ligand vaccine adjuvants, immunopotentiators. O'Hagan, Derek T., Schijns, Virgil, (eds.) Modern vaccines, 2nd ed., 2016, Elsevier.
33. [33] Zhao, B.G., Vasilakos, J.P., Tross, D., Smirnov, D., Klinman, D.M., Combination therapy targeting toll like receptors 7, 8 and 9 eliminates large established tumors. J Immunother Cancer, 2, 2014, 12.
34. [34] Singh, M., Khong, H., Dai, Z., Huang, X.-F., Wargo, J.A., Cooper, Z.A., et al. Effective innate and adaptive antimelanoma immunity through localized TLR7/8 activation. J Immunol Baltim Md 1950 193:9 (2014), 4722–4731.
35. [35] Orr MT, Fox CB, Baldwin SL, Sivananthan SJ, Lucas E, Lin S, et al. Adjuvant formulation structure and composition are critical for the development of an effective vaccine against tuberculosis. J Control Release Off J Control Release Soc [Internet]; 2013 November 28 [cited 2016 Feb 11], 172(1). Available from: < http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3871206/>.
36. [36] Guo, X., Stroup, S.E., Houpt, E.R., Persistence of Entamoeba histolytica infection in CBA mice owes to intestinal IL-4 production and inhibition of protective IFN-gamma. Mucosal Immunol 1:2 (2008), 139–146.
37. + DCs. Mucosal Immunol 8:4 (2015), 815–827.
38. [38] Hall, J.A., Cannons, J.L., Grainger, J.R., Santos, L.M.D., Hand, T.W., Naik, S., et al. Essential role for retinoic acid in the promotion of CD4+ T cell effector responses via retinoic acid receptor alpha. Immunity 34:3 (2011), 435–447.
39. [39] McCluskie, M.J., Weeratna, R.D., Payette, P.J., Davis, H.L., Parenteral and mucosal prime-boost immunization strategies in mice with hepatitis B surface antigen and CpG DNA. FEMS Immunol Med Microbiol 32:3 (2002), 179–185.
40. [40] Pattani, A., McKay, P.F., Garland, M.J., Curran, R.M., Migalska, K., Cassidy, C.M., et al. Microneedle mediated intradermal delivery of adjuvanted recombinant HIV-1 CN54gp140 effectively primes mucosal boost inoculations. J Control Release 162:3 (2012), 529–537.
41. [41] Lycke, N., Recent progress in mucosal vaccine development: potential and limitations. Nat Rev Immunol 12:8 (2012), 592–605.
42. [42] Fiorino F, Pettini E, Pozzi G, Medaglini D, Ciabattini A. Prime-boost strategies in mucosal immunization affect local IgA production and the type of Th response. Front Immunol [Internet]; 2013 May 29 [cited 2016 Feb 11];4. Available from: < http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3665932/>.
43. [43] Mora, J.R., Iwata, M., Eksteen, B., Song, S.-Y., Junt, T., Senman, B., et al. Generation of gut-homing IgA-secreting B cells by intestinal dendritic cells. Science 314:5802 (2006), 1157–1160.
44. [44] Abd Alla, M.D., Wolf, R., White, G.L., Kosanke, S.D., Cary, D., Verweij, J.J., et al. Efficacy of a Gal-lectin subunit vaccine against experimental Entamoeba histolytica infection and colitis in baboons (Papio sp.). Vaccine 30:20 (2012), 3068–3075.
45. [45] Owusu-Agyei, S., Ansong, D., Asante, K., Kwarteng Owusu, S., Owusu, R., Wireko Brobby, N.A., et al. Randomized controlled trial of RTS, S/AS02D and RTS, S/AS01E malaria candidate vaccines given according to different schedules in Ghanaian children. PLoS ONE, 4(10), 2009, e7302.
46. [46] Raverdeau, M., Mills, K.H.G., Modulation of T cell and innate immune responses by retinoic acid. J Immunol Baltim Md 1950 192:7 (2014), 2953–2958.
47. [47] Mwanza-Lisulo, M., Kelly, P., Potential for use of retinoic acid as an oral vaccine adjuvant. Phil Trans R Soc B, 370(1671), 2015, 20140145.
48. [48] Ross, A.C., Chen, Q., Ma, Y., Augmentation of antibody responses by retinoic acid and costimulatory molecules. Semin Immunol 21:1 (2009), 42–50.