Incorporation of a synthetic mycobacterial monomycoloyl glycerol analogue stabilizes dimethyldioctadecylammonium liposomes and potentiates their adjuvant effect in vivo

European Journal of Pharmaceutics and Biopharmaceutics

Volumn 77, Issue 1, 2011, Pages 89-98

  Nordly, Pernille ^a   Korsholm, Karen Smith ^b   Pedersen, Esra Alici ^a   Khilji, Tayba Sajid ^a   Franzyk, Henrik ^c   Jorgensen, Lene ^a   Nielsen, Hanne Mørck ^a   Agger, Else Marie ^b   Foged, Camilla ^a  

^a UNIVERSITY OF COPENHAGEN   (Denmark)

^b STATENS SERUM INSTITUT   (Denmark)

^c UNIVERSITY OF COPENHAGEN   (Denmark)

Author keywords

Adjuvant; Dimethyldioctadecylammonium; Liposome; Monomycoloyl glycerol; Nanomedicine; Vaccine

Indexed keywords

CONCANAVALIN A; DIMETHYLDIOCTADECYLAMMONIUM BROMIDE; IMMUNOGLOBULIN ANTIBODY; IMMUNOGLOBULIN G1 ANTIBODY; IMMUNOGLOBULIN G2C ANTIBODY; IMMUNOLOGICAL ADJUVANT; LIPOSOME; MONOMYCOLOYL GLYCEROL MMG 1; RECOMBINANT ANTIGEN; TUBERCULOSIS FUSION ANTIGEN AG85B ESAT 6; UNCLASSIFIED DRUG;

ADJUVANT THERAPY; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELLULAR IMMUNITY; COLLOID; CONTROLLED STUDY; DRUG DELIVERY SYSTEM; DRUG EFFECT; DRUG POTENTIATION; DRUG STABILITY; DRUG SYNTHESIS; FEMALE; HYDRATION; HYDROPHILICITY; IMMUNOGLOBULIN PRODUCTION; IMMUNOSTIMULATION; IN VIVO STUDY; LANGMUIR BLODGETT FILM; LIPID BILAYER; MOUSE; MYCOBACTERIUM; NONHUMAN; PARTICLE SIZE; PHASE TRANSITION; SURFACE TENSION; TH1 CELL; TH17 CELL; THERMAL ANALYSIS; TRANSITION TEMPERATURE; TRANSMISSION ELECTRON MICROSCOPY;

ACYLTRANSFERASES; ADJUVANTS, IMMUNOLOGIC; ANIMALS; ANTIGENS, BACTERIAL; BACTERIAL PROTEINS; COLLOIDS; DRUG STABILITY; FEMALE; IMMUNITY, CELLULAR; LIPOSOMES; MICE; MICE, INBRED C57BL; MONOGLYCERIDES; PARTICLE SIZE; PHYSICOCHEMICAL PHENOMENA; PRESERVATIVES, PHARMACEUTICAL; QUATERNARY AMMONIUM COMPOUNDS; RECOMBINANT FUSION PROTEINS; SURFACE PROPERTIES; SURFACE-ACTIVE AGENTS; T-LYMPHOCYTES, HELPER-INDUCER; TUBERCULOSIS VACCINES;

EID: 78650711244     PISSN: 09396411     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ejpb.2010.10.001     Document Type: Article

References (47)

1. B. Guy The perfect mix: recent progress in adjuvant research Nat. Rev. Microbiol. 5 2007 505 517
2. P. Nordly, H.B. Madsen, H.M. Nielsen, and C. Foged Status and future prospects of lipid-based particulate delivery systems as vaccine adjuvants and their combination with immunostimulators Expert Opin. Drug Deliv. 6 2009 657 672
3. D. Gall The adjuvant activity of aliphatic nitrogenous bases Immunology 11 1966 369 386
4. E.B. Lindblad, M.J. Elhay, R. Silva, R. Appelberg, and P. Andersen Adjuvant modulation of immune responses to tuberculosis subunit vaccines Infect. Immun. 65 1997 623 629
5. L. Brandt, M. Elhay, I. Rosenkrands, E.B. Lindblad, and P. Andersen ESAT-6 subunit vaccination against Mycobacterium tuberculosis Infect. Immun. 68 2000 791 795
6. C. Klinguer-Hamour, C. Libon, H. Plotnicky-Gilquin, M.C. Bussat, L. Revy, T. Nguyen, J.Y. Bonnefoy, N. Corvaia, and A. Beck DDA adjuvant induces a mixed Th1/Th2 immune response when associated with BBG2Na, a respiratory syncytial virus potential vaccine Vaccine 20 2002 2743 2751
7. J.P. Stanfield, D. Gall, and P.M. Bracken Single-dose antenatal tetanus immunisation Lancet 1 1973 215 219
8. L.A.T. Hilgers, M.W. Weststrate, Stabilized Adjuvant Suspension Comprising Dimethyldioctadecylammoniumbromide, US 5,026,546, 1991.
9. J. Davidsen, I. Rosenkrands, D. Christensen, A. Vangala, D. Kirby, Y. Perrie, E.M. Agger, and P. Andersen Characterization of cationic liposomes based on dimethyldioctadecylammonium and synthetic cord factor from M. tuberculosis (trehalose 6,6′-dibehenate) - a novel adjuvant inducing both strong CMI and antibody responses Biochim. Biophys. Acta 1718 2005 22 31
10. C.N. Sobral, M.A. Soto, and A.M. Carmona-Ribeiro Characterization of DODAB/DPPC vesicles Chem. Phys. Lipids 152 2008 38 45
11. D. Christensen, D. Kirby, C. Foged, E.M. Agger, P. Andersen, Y. Perrie, and H.M. Nielsen α,α′-Trehalose 6,6′-dibehenate in non-phospholipid-based liposomes enables direct interaction with trehalose, offering stability during freeze-drying Biochim. Biophys. Acta 1778 2008 1365 1373
12. E.M. Agger, I. Rosenkrands, J. Hansen, K. Brahimi, B.S. Vandahl, C. Aagaard, K. Werninghaus, C. Kirschning, R. Lang, D. Christensen, M. Theisen, F. Follmann, and P. Andersen Cationic liposomes formulated with synthetic mycobacterial cordfactor (CAF01): a versatile adjuvant for vaccines with different immunological requirements PLoS One 3 2008 e3116
13. A.W. Olsen, L.A.H. van Pinxteren, L.M. Okkels, P.B. Rasmussen, and P. Andersen Protection of mice with a tuberculosis subunit vaccine based on a fusion protein of antigen 85B and ESAT-6 Infect. Immun. 69 2001 2773 2778
14. D. Christensen, E.M. Agger, L.V. Andreasen, D. Kirby, P. Andersen, and Y. Perrie Liposome-based cationic adjuvant formulations (CAF): past, present, and future J. Liposome Res. 19 2009 2 11
15. R.E. Geisel, K. Sakamoto, D.G. Russell, and E.R. Rhoades In vivo activity of released cell wall lipids of Mycobacterium bovis bacillus Calmette-Guerin is due principally to trehalose mycolates J. Immunol. 174 2005 5007 5015
16. G.D. Sprott, C.J. Dicaire, K. Gurnani, S. Sad, and L. Krishnan Activation of dendritic cells by liposomes prepared from phosphatidylinositol mannosides from Mycobacterium bovis bacillus Calmette-Guerin and adjuvant activity in vivo Infect. Immun. 72 2004 5235 5246
17. I. Rosenkrands, E.M. Agger, A.W. Olsen, K.S. Korsholm, C.S. Andersen, K.T. Jensen, and P. Andersen Cationic liposomes containing mycobacterial lipids: a new powerful Th1 adjuvant system Infect. Immun. 73 2005 5817 5826
18. C.S. Andersen, E.M. Agger, I. Rosenkrands, J.M. Gomes, V. Bhowruth, K.J. Gibson, R.V. Petersen, D.E. Minnikin, G.S. Besra, and P. Andersen A simple mycobacterial monomycolated glycerol lipid has potent immunostimulatory activity J. Immunol. 182 2009 424 432
19. C.A. Andersen, I. Rosenkrands, A.W. Olsen, P. Nordly, D. Christensen, R. Lang, C. Kirschning, J.M. Gomes, V. Bhowruth, D.E. Minnikin, G.S. Besra, F. Follmann, P. Andersen, and E.M. Agger Novel generation mycobacterial adjuvant based on liposome-encapsulated monomycoloyl glycerol from Mycobacterium bovis bacillus Calmette-Guerin J. Immunol. 183 2009 2294 2302
20. V. Bhowruth, D.E. Minnikin, E.M. Agger, P. Andersen, V.W. Bramwell, Y. Perrie, and G.S. Besra Adjuvant properties of a simplified C32 monomycolyl glycerol analogue Bioorg. Med. Chem. Lett. 19 2009 2029 2032
21. A.K. Datta, K. Takayama, M.A. Nashed, and L. Anderson An improved synthesis of trehalose 6-mono- and 6,6′-di-corynomycolates and related esters Carbohydr. Res. 218 1991 95 109
22. L.J. Goosen, and A. Döhring A convenient protocol for the esterification of carboxylic acids with alcohols in the presence of di-t-butyl dicarbonate Synlett 2004 2004 263 266
23. R.T. Pon, S.Y. Yu, and Y.S. Sanghvi Rapid esterification of nucleosides to solid-phase supports for oligonucleotide synthesis using uronium and phosphonium coupling reagents Bioconjugate Chem. 10 1999 1051 1057
24. T. Yakura, Y. Yoshimoto, C. Ishida, and S. Mabuchi Synthesis of an immunomodulator (+)-conagenin and its analogs Tetrahedron 63 2007 4429 4438
25. A.J. Pearson, and M.V. Chelliah Synthesis of a model bicyclic CDE ring system of ristocetin A and observation of a facile inversion of configuration in a 16-membered DE ring model J. Org. Chem. 63 1998 3087 3098
26. E. Feitosa, and P.C.A. Barreleiro The effect of ionic strength on the structural organization of dioctadecyldimethylammonium bromide in aqueous solution Progr. Colloid Polym. Sci. 128 2004 163 168
27. E. Feitosa, G. Karlsson, and K. Edwards Unilamellar vesicles obtained by simply mixing dioctadecyldimethylammonium chloride and bromide with water Chem. Phys. Lipids 140 2006 66 74
28. M. Kepczynski, J. Bednar, D. Kuzmicz, P. Wydro, and M. Nowakowska Spontaneous formation of densely stacked multilamellar vesicles in dioctadecyldimethylammonium bromide/oleosiloxane mixtures Langmuir 26 2010 1551 1556
29. F.M. Linseisen, S. Bayerl, and T.M. Bayerl 2H-NMR and DSC study of DPPC-DODAB mixtures Chem. Phys. Lipids 83 1996 9 23
30. M.J. Blandamer, B. Briggs, P.M. Cullis, K.D. Irlam, S.D. Kirby, and J.B.F.N. Engberts Formation of vesicular bilayers in aqueous solutions containing mixtures of dialkyldimethylammonium bromides J. Mol. Liq. 75 1998 181 187
31. E. Feitosa, P.C. Barreleiro, and G. Olofsson Phase transition in dioctadecyldimethylammonium bromide and chloride vesicles prepared by different methods Chem. Phys. Lipids 105 2000 201 213
32. P.C.A. Barreleiro, G. Olofsson, W. Brown, K. Edwards, N.M. Bonassi, and E. Feitosa Interaction of octaethylene glycol n-dodecyl monoether with dioctadecyldimethylammonium bromide and chloride vesicles Langmuir 18 2002 1024 1029
33. A.M. Gonalves da Silva, and M.I. Viseu Synergism in mixed monolayers of cationic and anionic surfactants: a thermodynamic analysis of miscibility at the air-water interface Colloids Surf. A. Physicochem. Eng. Asp. 144 1998 191 200
34. D.T. O'Hagan, and E. De Gregorio The path to a successful vaccine adjuvant - 'the long and winding road' Drug Discov. Today 14 2009 541 551
35. C. Lonez, M. Vandenbranden, and J.M. Ruysschaert Cationic liposomal lipids: from gene carriers to cell signaling Prog. Lipid Res. 47 2008 340 347
36. K.S. Korsholm, E.M. Agger, C. Foged, D. Christensen, J. Dietrich, C.S. Andersen, C. Geisler, and P. Andersen The adjuvant mechanism of cationic dimethyldioctadecylammonium liposomes Immunology 121 2007 216 226
37. C.A. Kraaijeveld, G. la Riviere, B.J. Baissa-Trouw, J. Jansen, T. Harmsen, and H. Snippe Effect of the adjuvant dimethyl dioctadecyl ammonium bromide on the humoral and cellular immune responses to encephalomyocarditis virus Antiviral Res. 3 1983 137 149
38. J.R. Baldridge, P. McGowan, J.T. Evans, C. Cluff, S. Mossman, D. Johnson, and D. Persing Taking a Toll on human disease: Toll-like receptor 4 agonists as vaccine adjuvants and monotherapeutic agents Expert Opin. Biol. Ther. 4 2004 1129 1138
39. G.R. Olds, L. Chedid, E. Lederer, and A.A. Mahmoud Induction of resistance to Schistosoma mansoni by natural cord factor and synthetic lower homologues J. Infect. Dis. 141 1980 473 478
40. M.V. Pimm, R.W. Baldwin, J. Polonsky, and E. Lederer Immunotherapy of an ascitic rat hepatoma with cord factor (trehalose-6,6′-dimycolate) and synthetic analogues Int. J. Cancer 24 1979 780 785
41. G. Cevc How membrane chain-melting phase-transition temperature is affected by the lipid chain asymmetry and degree of unsaturation: an effective chain-length model Biochemistry 30 1991 7186 7193
42. D.A. Mannock, R.N. Lewis, R.N. McElhaney, P.E. Harper, D.C. Turner, and S.M. Gruner An analysis of the relationship between fatty acid composition and the lamellar gel to liquid-crystalline and the lamellar to inverted nonlamellar phase transition temperatures of phosphatidylethanolamines and diacyl-alpha-d-glucosyl glycerols Eur. Biophys. J. 30 2001 537 554
43. D. Marsh General features of phospholipid phase transitions Chem. Phys. Lipids 57 1991 109 120
44. G. Cevc, A. Watts, and D. Marsh Titration of the phase transition of phosphatidylserine bilayer membranes. Effects of pH, surface electrostatics, ion binding, and head-group hydration Biochemistry 20 1981 4955 4965
45. G. Cevc Isothermal lipid phase transitions Chem. Phys. Lipids 57 1991 293 307
46. O. Bakouche, and D. Gerlier Enhancement of immunogenicity of tumour virus antigen by liposomes: the effect of lipid composition Immunology 58 1986 507 513
47. T. Yasuda, G.F. Dancey, and S.C. Kinsky Immunogenicity of liposomal model membranes in mice: dependence on phospholipid composition Proc. Natl. Acad. Sci. USA 74 1977 1234 1236