Liposomal vaccines incorporating molecular adjuvants and intrastructural T-cell help promote the immunogenicity of HIV membrane-proximal external region peptides

Vaccine

Volumn 33, Issue 7, 2015, Pages 861-868

  Hanson, Melissa C ^a,b   Abraham, Wuhbet ^b   Crespo, Monica P ^b   Chen, Stephanie H ^a   Liu, Haipeng ^b   Szeto, Greg Lee ^a,b   Kim, Mikyung ^d   Reinherz, Ellis L ^d   Irvine, Darrell J ^a,b,c  

^a USA   (United States)

^b MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^c HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^d DANA FARBER CANCER INSTITUTE   (United States)

Author keywords

Adjuvant; HIV vaccine; Lipid membrane; Liposome; MPER; Nanoparticle

Indexed keywords

ADDAVAX; ALUMINUM POTASSIUM SULFATE; HUMAN IMMUNODEFICIENCY VIRUS VACCINE; IMMUNOGLOBULIN G; IMMUNOLOGICAL ADJUVANT; INTERLEUKIN 4; INTERLEUKIN 5; LIPOSOME; MEMBRANE PROXIMAL EXTERNAL REGION PEPTIDE VACCINE; MONTANIDE ISA 51; PEPTIDE VACCINE; PHOSPHORYL LIPID A; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; WATER OIL CREAM; GLYCOPROTEIN GP 41; NANOPARTICLE;

ADJUVANT THERAPY; ANTIBODY RESPONSE; ARTICLE; B LYMPHOCYTE; CONFOCAL MICROSCOPY; CRYOELECTRON MICROSCOPY; CYTOKINE RELEASE; CYTOKINE RESPONSE; ENCAPSULATION; FEMALE; FLOW CYTOMETRY; HUMORAL IMMUNITY; IMMUNE RESPONSE; IMMUNIZATION; IMMUNOGENICITY; INGUINAL LYMPH NODE; LIPID MEMBRANE; LIPOSOMAL DELIVERY; MEMBRANE FLUIDITY; MOUSE; NONHUMAN; PARTICLE SIZE; PRIORITY JOURNAL; T LYMPHOCYTE; ANIMAL; ANTIBODY PRODUCTION; BAGG ALBINO MOUSE; CHEMISTRY; IMMUNOLOGY;

AIDS VACCINES; ANIMALS; ANTIBODY FORMATION; FEMALE; HIV ENVELOPE PROTEIN GP41; LIPOSOMES; MICE; MICE, INBRED BALB C; NANOPARTICLES; T-LYMPHOCYTES;

EID: 84921718712     PISSN: 0264410X     EISSN: 18732518     Source Type: Journal    
DOI: 10.1016/j.vaccine.2014.12.045     Document Type: Article

References (50)

1. McCoy L.E., Weiss R.A. Neutralizing antibodies to HIV-1 induced by immunization. J Exp Med 2013, 210:209-223.
2. Zolla-Pazner S. A critical question for HIV vaccine development: which antibodies to induce?. Science 2014, 345:167-168.
3. Balazs A.B., Chen J., Hong C.M., Rao D.S., Yang L., Baltimore D. Antibody-based protection against HIV infection by vectored immunoprophylaxis. Nature 2012, 481:81-84.
4. McElrath M.J., Haynes B.F. Induction of immunity to human immunodeficiency virus type-1 by vaccination. Immunity 2010, 33:542-554.
5. Kwong P.D., Doyle M.L., Casper D.J., Cicalak C., Leavitt S.A., Majeed S., et al. HIV-1 evades antibody-mediated neutralization through conformational masking of receptor-binding sites. Nature 2002, 420:678-682.
6. Haynes B., Shattock R. Critical issues in mucosal immunity for HIV-1 vaccine development. J Allergy Clin Immunol 2008, 122:3-11.
7. Muster T., Steindl F., Purtscher M., Trkola A., Klima A., Himmler G., et al. A conserved neutralizing epitope on gp41 of human immunodeficiency virus type 1. J Virol 1993, 67:6642-6647.
8. Nelson J.D., Brunel F.M., Jensen R., Crooks E.T., Cardoso R.M.F., Wang M., et al. An affinity-enhanced neutralizing antibody against the membrane-proximal external region of human immunodeficiency virus type 1 gp41 recognizes an epitope between those of 2F5 and 4E10. J Virol 2007, 81:4033-4043.
9. Zwick M.B., Labrijn A.F., Wang M., Spenlehauer C., Saphire E.O., Binley J.M., et al. Broadly neutralizing antibodies targeted to the membrane-proximal external region of human immunodeficiency virus type 1 glycoprotein gp41. J Virol 2001, 75:10892-10905.
10. Stiegler G., Kunert R., Purtscher M., Wolbank S., Voglauer R., Steindl F., et al. A potent cross-clade neutralizing human monoclonal antibody against a novel epitope on gp41 of human immunodeficiency virus type 1. AIDS Res Hum Retroviruses 2001, 17:1757-1765.
11. Huang J., Ofek G., Laub L., Louder M.K., Doria-Rose N.A., Longo N.S., et al. Broad and potent neutralization of HIV-1 by a gp41-specific human antibody. Nature 2012, 491:406-412.
12. Sun Z-Y.J., Oh K.J., Kim M., Yu J., Brusic V., Song L., et al. HIV-1 broadly neutralizing antibody extracts its epitope from a kinked gp41 ectodomain region on the viral membrane. Immunity 2008, 28:52-63.
13. Kim M., Sun Z-Y.J., Rand K.D., Shi X., Song L., Cheng Y., et al. Antibody mechanics on a membrane-bound HIV segment essential for GP41-targeted viral neutralization. Nat Struct Mol Biol 2011, 18:1235-1243.
14. Song L., Sun Z-Y.J., Coleman K.E., Zwick M.B., Gach J.S., Wang J., et al. Broadly neutralizing anti-HIV-1 antibodies disrupt a hinge-related function of gp41 at the membrane interface. Proc Natl Acad Sci USA 2009, 106:9057-9062.
15. Montero M., van Houten N.E., Wang X., Scott J.K. The membrane-proximal external region of the human immunodeficiency virus type 1 envelope: dominant site of antibody neutralization and target for vaccine design. Microbiol Mol Biol Rev 2008, 72:54-84.
16. Gach J.S., Leaman D.P., Zwick M.B. Targeting HIV-1 gp41 in close proximity to the membrane using antibody and other molecules. Curr Top Med Chem 2011, 11:2997-3021.
17. Coëffier E., Clément J.M., Cussac V., Khodaei-Boorane N., Jehanno M., Rojas M., et al. Antigenicity and immunogenicity of the HIV-1 gp41 epitope ELDKWA inserted into permissive sites of the MalE protein. Vaccine 2000, 19:684-693.
18. Correia B.E., Ban Y-E.A., Holmes M.A., Xu H., Ellingson K., Kraft Z., et al. Computational design of epitope-scaffolds allows induction of antibodies specific for a poorly immunogenic HIV vaccine epitope. Structure 2010, 18:1116-1126.
19. Law M., Cardoso R.M.F., Wilson I.a., Burton D.R. Antigenic and immunogenic study of membrane-proximal external region-grafted gp120 antigens by a DNA prime-protein boost immunization strategy. J Virol 2007, 81:4272-4285.
20. Ofek G., Guenaga F.J., Schief W.R., Skinner J., Baker D., Wyatt R., et al. Elicitation of structure-specific antibodies by epitope scaffolds. Proc Natl Acad Sci USA 2010, 107:17880-17887.
21. Hinz A., Schoehn G., Quendler H., Hulsik D.L., Stiegler G., Katinger H., et al. Characterization of a trimeric MPER containing HIV-1 gp41 antigen. Virology 2009, 390:221-227.
22. Kim M., Qiao Z., Yu J., Montefiori D., Reinherz E.L. Immunogenicity of recombinant human immunodeficiency virus type 1-like particles expressing gp41 derivatives in a pre-fusion state. Vaccine 2007, 25:5102-5114.
23. Kamdem Toukam D., Tenbusch M., Stang A., Temchura V., Storcksdieck Genannt Bonsmann M., Grewe B., et al. Targeting antibody responses to the membrane proximal external region of the envelope glycoprotein of human immunodeficiency virus. PLoS One 2012, 7:e38068.
24. Pastori C., Tudor D., Diomede L., Drillet A.S., Jegerlehner A., Röhn T.A., et al. Virus like particle based strategy to elicit HIV-protective antibodies to the alpha-helic regions of gp41. Virology 2012, 431:1-11.
25. Matyas G.R., Wieczorek L., Beck Z., Ochsenbauer-Jambor C., Kappes J.C., Michael N.L., et al. Neutralizing antibodies induced by liposomal HIV-1 glycoprotein 41 peptide simultaneously bind to both the 2F5 or 4E10 epitope and lipid epitopes. AIDS 2009, 23:2069-2077.
26. Zhang J., Alam S.M., Bouton-Verville H., Chen Y., Newman A., Stewart S., et al. Modulation of nonneutralizing HIV-1 gp41 responses by an MHC-restricted TH epitope overlapping those of membrane proximal external region broadly neutralizing antibodies. J Immunol 2014, 192:1693-1706.
27. Dennison S.M., Sutherland L.L., Jaeger F.H., Anasti K.M., Parks R., Stewart S., et al. Induction of antibodies in Rhesus Macaques that recognize a fusion-intermediate conformation of HIV-1 gp41. PLoS One 2011, 6:e27824.
28. Venditto V.J., Watson D.S., Motion M., Montefiori D., Szoka F.C. Rational design of membrane proximal external region lipopeptides containing chemical modifications for HIV-1 vaccination. Clin Vaccine Immunol 2013, 20:39-45.
29. Kim M., Song L., Moon J., Sun Z-Y.J., Bershteyn A., Hanson M., et al. Immunogenicity of membrane-bound HIV-1 gp41 membrane-proximal external region (MPER) segments is dominated by residue accessibility and modulated by stereochemistry. J Biol Chem 2013, 288:31888-31901.
30. Watson D.S., Szoka F.C. Role of lipid structure in the humoral immune response in mice to covalent lipid-peptides from the membrane proximal region of HIV-1 gp41. Vaccine 2009, 27:4672-4683.
31. Ahsan F. Targeting to macrophages: role of physicochemical properties of particulate carriers - liposomes and microspheres - on the phagocytosis by macrophages. J Control Release 2002, 79:29-40.
32. Bachmann M.F., Jennings G.T. Vaccine delivery: a matter of size, geometry, kinetics and molecular patterns. Nat Rev Immunol 2010, 10:787-796.
33. Liu H., Zhu Z., Kang H., Wu Y., Sefan K., Tan W. DNA-based micelles: synthesis, micellar properties and size-dependent cell permeability. Chemistry 2010, 16:3791-3797.
34. Fox C.B., Haensler J. An update on safety and immunogenicity of vaccines containing emulsion-based adjuvants. Expert Rev Vaccines 2013, 12:747-758.
35. Alving C.R., Rao M., Steers N.J., Matyas G.R., Mayorov A.V. Liposomes containing lipid A: an effective, safe, generic adjuvant system for synthetic vaccines. Expert Rev Vaccines 2012, 11:733-744.
36. Libanova R., Becker P.D., Guzmán C.a. Cyclic di-nucleotides: new era for small molecules as adjuvants. Microb Biotechnol 2012, 5:168-176.
37. Shu C., Yi G., Watts T., Kao C.C., Li P. Structure of STING bound to cyclic di-GMP reveals the mechanism of cyclic dinucleotide recognition by the immune system. Nat Struct Mol Biol 2012, 19:722-724.
38. Madhun A.S., Haaheim L.R., Nøstbakken J.K., Ebensen T., Chichester J., Yusibov V., et al. Intranasal c-di-GMP-adjuvanted plant-derived H5 influenza vaccine induces multifunctional Th1 CD4+ cells and strong mucosal and systemic antibody responses in mice. Vaccine 2011, 29:4973-4982.
39. Dos Santos N., Allen C., Doppen A.-M., Anantha M., Cox K.a K., Gallagher R.C., et al. Influence of poly(ethylene glycol) grafting density and polymer length on liposomes: relating plasma circulation lifetimes to protein binding. Biochim Biophys Acta 2007, 1768:1367-1377.
40. Bestman-Smith J., Gourde P., Désormeaux A., Tremblay M.J., Bergeron M.G. Sterically stabilized liposomes bearing anti-HLA-DR antibodies for targeting the primary cellular reservoirs of HIV-1. Biochim Biophys Acta-Biomembr 2000, 1468:161-174.
41. Moghimi S.M. The effect of methoxy-PEG chain length and molecular architecture on lymph node targeting of immuno-PEG liposomes. Biomaterials 2006, 27:136-144.
42. Oyewumi M.O., Kumar A., Cui Z. Nano-microparticles as immune adjuvants: correlating particle sizes and the resultant immune responses. Expert Rev Vaccines 2010, 9:1095-1107.
43. Oussoren C., Zuidema J., Crommelin D.J.A., Storm G. Lymphatic uptake and biodistribution of liposomes after subcutaneous injection. II. Influence of liposomal size, lipid composition and lipid dose. Biochim Biophys Acta-Biomembr 1997, 1328:261-272.
44. Watson D.S., Endsley A.N., Huang L. Design considerations for liposomal vaccines: influence of formulation parameters on antibody and cell-mediated immune responses to liposome associated antigens. Vaccine 2012, 30:2256-2272.
45. Dancey G.F., Yasuda T., Kinsky S.C. Effect of liposomal model membrane composition on immunogenicity. J Immunol 1978, 120:1109-1113.
46. Bakouche O., Gerlier D. Enhancement of immunogenicity of tumour virus antigen by liposomes: the effect of lipid composition. Immunology 1986, 58:507-513.
47. Ghasparian A., Riedel T., Koomullil J., Moehle K., Gorba C., Svergun D.I., et al. Engineered synthetic virus-like particles and their use in vaccine delivery. ChemBioChem 2011, 12:100-109.
48. Puffer E.B., Pontrello J.K., Hollenbeck J.J., Kink J.A., Kiessling L.L. Activating B cell signaling with defined multivalent ligands. ACS Chem Biol 2007, 2:252-262.
49. Lazarski C.A., Chaves F.A., Jenks S.A., Wu S., Richards K.A., Weaver J.M., et al. The kinetic stability of MHC class II: peptide complexes is a key parameter that dictates immunodominance. Immunity 2005, 23:29-40.
50. Dai G., Steede N.K., Landry S.J. Allocation of helper T-cell epitope immunodominance according to three-dimensional structure in the human immunodeficiency virus type I envelope glycoprotein gp120. J Biol Chem 2001, 276:41913-41920.