Site-specific incorporation of three toll-like receptor 2 targeting adjuvants into semisynthetic, molecularly defined nanoparticles: Application to group a streptococcal vaccines

Bioconjugate Chemistry

Volumn 25, Issue 5, 2014, Pages 965-978

  Moyle, Peter M ^a   Dai, Wei ^a   Zhang, Yingkai ^a   Batzloff, Michael R ^b   Good, Michael F ^b   Toth, Istvan ^a  

^a UNIVERSITY OF QUEENSLAND   (Australia)

^b GRIFFITH UNIVERSITY   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIBODIES; CELL MEMBRANES; EPITOPES; LIGANDS; NANOPARTICLES; PEPTIDES; RECOMBINANT PROTEINS; SITE SELECTION;

LIPID CORES; N-TERMINALS; NANOPARTICLE APPLICATIONS; OPTIMISATIONS; PROPERTY; PROTEIN ANTIGENS; SITE-SPECIFIC; SUBUNIT VACCINE; SYNTHETIC PEPTIDE; TOLL-LIKE RECEPTOR 2;

VACCINES;

DIPALMITOYL S GLYCERYL CYSTEINE VACCINE; IMMUNOGLOBULIN G ANTIBODY; IMMUNOLOGICAL ADJUVANT; J14 ANTIGEN; LIPID CORE PEPTIDE VACCINE; NANOPARTICLE; PEPTIDE VACCINE; RECOMBINANT ANTIGEN; RECOMBINANT PROTEIN; STREPTOCOCCUS VACCINE; SYNTHETIC PEPTIDE; TOLL LIKE RECEPTOR 2; TRIPALMITOYL S GLYCEROL CYSTEINE VACCINE; UNCLASSIFIED DRUG; LIGAND; TLR2 PROTEIN, HUMAN;

ADJUVANT THERAPY; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIBODY BLOOD LEVEL; ANTIBODY RESPONSE; ANTIBODY TITER; ANTIGEN BINDING; ANTIGEN EXPRESSION; ANTIGEN SPECIFICITY; ARTICLE; CELL SURFACE; CONTROLLED STUDY; DRUG CONJUGATION; DRUG EFFICACY; DRUG FORMULATION; DRUG POTENCY; DRUG SOLUBILITY; DRUG STABILITY; DRUG SYNTHESIS; GROUP A STREPTOCOCCAL INFECTION; IMMUNE RESPONSE; IMMUNOSTIMULATION; MOUSE; NANOMEDICINE; NONHUMAN; PEPTIDE SYNTHESIS; PROTEIN ENGINEERING; SOLID PHASE SYNTHESIS; STREPTOCOCCUS GROUP A; STREPTOCOCCUS PYOGENES; VACCINATION; VACCINE PRODUCTION; AGONISTS; ANIMAL; C57BL MOUSE; CHEMICAL STRUCTURE; CHEMISTRY; DOSE RESPONSE; HUMAN; IMMUNOLOGY; MICROBIAL SENSITIVITY TEST; PARTICLE SIZE; STRUCTURE ACTIVITY RELATION; SURFACE PROPERTY; SYNTHESIS;

ANIMALS; DOSE-RESPONSE RELATIONSHIP, DRUG; HUMANS; LIGANDS; MICE; MICE, INBRED C57BL; MICROBIAL SENSITIVITY TESTS; MOLECULAR STRUCTURE; NANOPARTICLES; PARTICLE SIZE; STREPTOCOCCAL VACCINES; STREPTOCOCCUS PYOGENES; STRUCTURE-ACTIVITY RELATIONSHIP; SURFACE PROPERTIES; TOLL-LIKE RECEPTOR 2;

EID: 84901009955     PISSN: 10431802     EISSN: 15204812     Source Type: Journal    
DOI: 10.1021/bc500108b     Document Type: Article

References (60)

1. Pulendran, B. and Ahmed, R. (2011) Immunological mechanisms of vaccination Nat. Immunol. 12, 509-517
2. Rueckert, C. and Guzman, C. A. (2012) Vaccines: from empirical development to rational design PLoS Pathol. 8, e1003001
3. Moyle, P. M. and Toth, I. (2013) Modern subunit vaccines: development, components, and research opportunities ChemMedChem 8, 360-376
4. Reed, S. G., Orr, M. T., and Fox, C. B. (2013) Key roles of adjuvants in modern vaccines Nat. Med. 19, 1597-1608
5. Schmidt, J., Welsch, T., Jager, D., Muhlradt, P. F., Buchler, M. W., and Marten, A. (2007) Intratumoural injection of the Toll-like receptor-2/6 agonist macrophage-activating lipopeptide-2 in patients with pancreatic carcinoma: a phase I/II trial Br. J. Cancer 97, 598-604
6. Seth, A., Yasutomi, Y., Jacoby, H., Callery, J. C., Kaminsky, S. M., Koff, W. C., Nixon, D. F., and Letvin, N. L. (2000) Evaluation of a lipopeptide immunogen as a therapeutic in HIV type 1-seropositive individuals AIDS Res. Hum. Retroviruses 16, 337-343
7. Richmond, P. C., Marshall, H. S., Nissen, M. D., Jiang, Q., Jansen, K. U., Garces-Sanchez, M., Martinon-Torres, F., Beeslaar, J., Szenborn, L., Wysocki, J., Eiden, J., Harris, S. L., Jones, T. R., and Perez, J. L. (2012) Safety, immunogenicity, and tolerability of meningococcal serogroup B bivalent recombinant lipoprotein 2086 vaccine in healthy adolescents: a randomised, single-blind, placebo-controlled, phase 2 trial Lancet Infect. Dis. 12, 597-607
8. Salunke, D. B., Connelly, S. W., Shukla, N. M., Hermanson, A. R., Fox, L. M., and David, S. A. (2013) Design and development of stable, water-soluble, human Toll-like receptor 2 specific monoacyl lipopeptides as candidate vaccine adjuvants J. Med. Chem. 56, 5885-5900
9. Agnihotri, G., Crall, B. M., Lewis, T. C., Day, T. P., Balakrishna, R., Warshakoon, H. J., Malladi, S. S., and David, S. A. (2011) Structure-activity relationships in Toll-like receptor 2-agonists leading to simplified monoacyl lipopeptides J. Med. Chem. 54, 8148-8160
10. Zhu, X., Ramos, T. V., Gras-Masse, H., Kaplan, B. E., and BenMohamed, L. (2004) Lipopeptide epitopes extended by an N-palmitoyl-lysine moiety increase uptake and maturation of dendritic cells through a Toll-like receptor-2 pathway and trigger a Th1-dependent protective immunity Eur. J. Immunol. 34, 3102-3114
11. Zom, G. G., Khan, S., Filippov, D. V., and Ossendorp, F. (2012) TLR ligand-peptide conjugate vaccines: toward clinical application Adv. Immunol. 114, 177-201
12. Boato, F., Thomas, R. M., Ghasparian, A., Freund-Renard, A., Moehle, K., and Robinson, J. A. (2007) Synthetic virus-like particles from self-assembling coiled-coil lipopeptides and their use in antigen display to the immune system Angew. Chem., Int. Ed. 46, 9015-9018
13. Moyle, P. M., Hartas, J., Henningham, A., Batzloff, M. R., Good, M. F., and Toth, I. (2013) An efficient, chemically-defined semisynthetic lipid-adjuvanted nanoparticulate vaccine development system Nanomed. Nanotechnol. Biol. Med. 9, 935-944
14. Smith, D. M., Simon, J. K., and Baker, J. R., Jr. (2013) Applications of nanotechnology for immunology Nat. Rev. Immunol. 13, 592-605
15. Bachmann, M. F. and Jennings, G. T. (2010) Vaccine delivery: a matter of size, geometry, kinetics and molecular patterns Nat. Rev. Immunol. 10, 787-796
16. Chua, B. Y., Zeng, W., and Jackson, D. C. (2008) Synthesis of Toll-like receptor-2 targeting lipopeptides as self-adjuvanting vaccines Methods Mol. Biol. 494, 247-261
17. Abdel-Aal, A. B., Zaman, M., Fujita, Y., Batzloff, M. R., Good, M. F., and Toth, I. (2010) Design of three-component vaccines against group A streptococcal infections: importance of spatial arrangement of vaccine components J. Med. Chem. 53, 8041-8046
18. Ragupathi, G., Koide, F., Livingston, P. O., Cho, Y. S., Endo, A., Wan, Q., Spassova, M. K., Keding, S. J., Allen, J., Ouerfelli, O., Wilson, R. M., and Danishefsky, S. J. (2006) Preparation and evaluation of unimolecular pentavalent and hexavalent antigenic constructs targeting prostate and breast cancer: a synthetic route to anticancer vaccine candidates J. Am. Chem. Soc. 128, 2715-2725
19. Kent, S. B. (2009) Total chemical synthesis of proteins Chem. Soc. Rev. 38, 338-351
20. Dale, J. B., Penfound, T. A., Chiang, E. Y., and Walton, W. J. (2011) New 30-valent M protein-based vaccine evokes cross-opsonic antibodies against non-vaccine serotypes of group A streptococci Vaccine 29, 8175-8178
21. Brandt, E. R., Sriprakash, K. S., Hobb, R. I., Hayman, W. A., Zeng, W., Batzloff, M. R., Jackson, D. C., and Good, M. F. (2000) New multi-determinant strategy for a group A streptococcal vaccine designed for the Australian Aboriginal population Nat. Med. 6, 455-459
22. Zeng, W., Eriksson, E. M., Lew, A., and Jackson, D. C. (2011) Lipidation of intact proteins produces highly immunogenic vaccine candidates Mol. Immunol. 48, 490-496
23. Chen, H. W., Liu, S. J., Liu, H. H., Kwok, Y., Lin, C. L., Lin, L. H., Chen, M. Y., Tsai, J. P., Chang, L. S., Chiu, F. F., Lai, L. W., Lian, W. C., Yang, C. Y., Hsieh, S. Y., Chong, P., and Leng, C. H. (2009) A novel technology for the production of a heterologous lipoprotein immunogen in high yield has implications for the field of vaccine design Vaccine 27, 1400-1409
24. Steer, A. C., Dale, J. B., and Carapetis, J. R. (2013) Progress toward a global group A streptococcal vaccine Pediatr. Infect. Dis. J. 32, 180-182
25. Zeng, W., Azzopardi, K., Hocking, D., Wong, C. Y., Robevska, G., Tauschek, M., Robins-Browne, R. M., and Jackson, D. C. (2012) A totally synthetic lipopeptide-based self-adjuvanting vaccine induces neutralizing antibodies against heat-stable enterotoxin from enterotoxigenic Escherichia coli Vaccine 30, 4800-4806
26. Zeng, W., Jackson, D. C., Murray, J., Rose, K., and Brown, L. E. (2000) Totally synthetic lipid-containing polyoxime peptide constructs are potent immunogens Vaccine 18, 1031-9
27. Zaman, M., Abdel-Aal, A. B., Fujita, Y., Phillipps, K. S., Batzloff, M. R., Good, M. F., and Toth, I. (2012) Immunological evaluation of lipopeptide group A streptococcus (GAS) vaccine: structure-activity relationship PloS One 7, e30146
28. Curiel, T. J., Morris, C., Brumlik, M., Landry, S. J., Finstad, K., Nelson, A., Joshi, V., Hawkins, C., Alarez, X., Lackner, A., and Mohamadzadeh, M. (2004) Peptides identified through phage display direct immunogenic antigen to dendritic cells J. Immunol. 172, 7425-7431
29. Alexander, J., Sidney, J., Southwood, S., Ruppert, J., Oseroff, C., Maewal, A., Snoke, K., Serra, H. M., Kubo, R. T., Sette, A., and Grey, H. M. (1994) Development of high potency universal DR-restricted helper epitopes by modification of high affinity DR-blocking peptides Immunity 1, 751-761
30. Zaman, M., Abdel-Aal, A. B., Phillipps, K. S., Fujita, Y., Good, M. F., and Toth, I. (2010) Structure-activity relationship of lipopeptide Group A streptococcus (GAS) vaccine candidates on Toll-like receptor 2 Vaccine 28, 2243-2248
31. Kang, J. Y., Nan, X., Jin, M. S., Youn, S. J., Ryu, Y. H., Mah, S., Han, S. H., Lee, H., Paik, S. G., and Lee, J. O. (2009) Recognition of lipopeptide patterns by Toll-like receptor 2-Toll-like receptor 6 heterodimer Immunity 31, 873-884
32. Jin, M. S., Kim, S. E., Heo, J. Y., Lee, M. E., Kim, H. M., Paik, S. G., Lee, H., and Lee, J. O. (2007) Crystal structure of the TLR1-TLR2 heterodimer induced by binding of a tri-acylated lipopeptide Cell 130, 1071-1082
33. Shen, B. Q., Xu, K., Liu, L., Raab, H., Bhakta, S., Kenrick, M., Parsons-Reponte, K. L., Tien, J., Yu, S. F., Mai, E., Li, D., Tibbitts, J., Baudys, J., Saad, O. M., Scales, S. J., McDonald, P. J., Hass, P. E., Eigenbrot, C., Nguyen, T., Solis, W. A., Fuji, R. N., Flagella, K. M., Patel, D., Spencer, S. D., Khawli, L. A., Ebens, A., Wong, W. L., Vandlen, R., Kaur, S., Sliwkowski, M. X., Scheller, R. H., Polakis, P., and Junutula, J. R. (2012) Conjugation site modulates the in vivo stability and therapeutic activity of antibody-drug conjugates Nat. Biotechnol. 30, 184-189
34. Baldwin, A. D. and Kiick, K. L. (2011) Tunable degradation of maleimide-thiol adducts in reducing environments Bioconjugate Chem. 22, 1946-1953
35. Hermanson, G. T. (2013) Bioconjugate Techniques, 3 rd ed., Academic Press, London.
36. Evans, T. C., Jr., Benner, J., and Xu, M. Q. (1998) Semisynthesis of cytotoxic proteins using a modified protein splicing element Protein Sci. 7, 2256-2264
37. Muir, T. W., Sondhi, D., and Cole, P. A. (1998) Expressed protein ligation: a general method for protein engineering Proc. Natl. Acad. Sci. U.S.A. 95, 6705-6710
38. Dawson, P. E., Muir, T. W., Clark-Lewis, I., and Kent, S. B. (1994) Synthesis of proteins by native chemical ligation Science 266, 776-779
39. Zeng, W., Ghosh, S., Lau, Y. F., Brown, L. E., and Jackson, D. C. (2002) Highly immunogenic and totally synthetic lipopeptides as self-adjuvanting immunocontraceptive vaccines J. Immunol. 169, 4905-4912
40. α-Fmoc protected derivatives of S -(2,3-dihydroxypropyl)- cysteine and their application in peptide synthesis Int. J. Pept. Protein Res. 38, 545-554
41. Li, Y. M., Yongye, A., Giulianotti, M., Martinez-Mayorga, K., Yu, Y. P., and Houghten, R. A. (2009) Synthesis of cyclic peptides through direct aminolysis of peptide thioesters catalyzed by imidazole in aqueous organic solutions J. Comb. Chem. 11, 1066-1072
42. Blaschke, U. K., Silberstein, J., and Muir, T. W. (2000) Protein engineering by expressed protein ligation Methods Enzymol. 328, 478-496
43. Johnson, E. C. and Kent, S. B. (2006) Insights into the mechanism and catalysis of the native chemical ligation reaction J. Am. Chem. Soc. 128, 6640-6646
44. Wan, Q. and Danishefsky, S. J. (2007) Free-radical-based, specific desulfurization of cysteine: A powerful advance in the synthesis of polypeptides and glycopolypeptides Angew. Chem., Int. Ed. 46, 9248-9252
45. Lycke, N. (2012) Recent progress in mucosal vaccine development: potential and limitations Nat. Rev. Immunol. 12, 592-605
46. Georgousakis, M. M., McMillan, D. J., Batzloff, M. R., and Sriprakash, K. S. (2009) Moving forward: a mucosal vaccine against group A streptococcus Expert Rev. Vaccines. 8, 747-760
47. Moyle, P. M., Olive, C., Ho, M. F., Good, M. F., and Toth, I. (2006) Synthesis of a highly pure lipid core peptide based self-adjuvanting triepitopic group A streptococcal vaccine, and subsequent immunological evaluation J. Med. Chem. 49, 6364-6370
48. Vohra, H., Dey, N., Gupta, S., Sharma, A. K., Kumar, R., McMillan, D., and Good, M. F. (2005) M protein conserved region antibodies opsonise multiple strains of Streptococcus pyogenes with sequence variations in C-repeats Res. Microbiol. 156, 575-582
49. Batzloff, M. R., Hayman, W. A., Davies, M. R., Zeng, M., Pruksakorn, S., Brandt, E. R., and Good, M. F. (2003) Protection against group A streptococcus by immunization with J8-diphtheria toxoid: contribution of J8- and diphtheria toxoid-specific antibodies to protection J. Infect. Dis. 187, 1598-1608
50. Hayman, W. A., Brandt, E. R., Relf, W. A., Cooper, J., Saul, A., and Good, M. F. (1997) Mapping the minimal murine T cell and B cell epitopes within a peptide vaccine candidate from the conserved region of the M protein of group A streptococcus Int. Immunol. 9, 1723-1733
51. Siegrist, C.-A. (2008) Vaccine immunology, in Vaccines (Plotkin, S. A., Orenstein, W. A., and Offit, P. A., Eds.) pp 18-36, Saunders, Philadelphia.
52. Steer, A. C., Batzloff, M. R., Mulholland, K., and Carapetis, J. R. (2009) Group A streptococcal vaccines: facts versus fantasy Curr. Opin. Infect. Dis. 22, 544-552
53. Schittek, B. and Rajewsky, K. (1990) Maintenance of B-cell memory by long-lived cells generated from proliferating precursors Nature 346, 749-751
54. Sprent, J. and Tough, D. F. (1994) Lymphocyte life-span and memory Science 265, 1395-1400
55. Pandey, M., Wykes, M. N., Hartas, J., Good, M. F., and Batzloff, M. R. (2013) Long-term antibody memory induced by synthetic peptide vaccination is protective against Streptococcus pyogenes infection and Is independent of memory T cell help J. Immunol. 190, 2692-2701
56. Cole, J. N., Barnett, T. C., Nizet, V., and Walker, M. J. (2011) Molecular insight into invasive group A streptococcal disease Nat. Rev. Microbiol. 9, 724-736
57. Steer, A. C., Law, I., Matatolu, L., Beall, B. W., and Carapetis, J. R. (2009) Global emm type distribution of group A streptococci: systematic review and implications for vaccine development Lancet Infect. Dis. 9, 611-616
58. Dale, J. B., Fischetti, V. A., Carapetis, J. R., Steer, A. C., Sow, S., Kumar, R., Mayosi, B. M., Rubin, F. A., Mulholland, K., Hombach, J. M., Schodel, F., and Henao-Restrepo, A. M. (2013) Group A streptococcal vaccines: paving a path for accelerated development Vaccine 31, B216-B222
59. McMillan, D. J., Dreze, P. A., Vu, T., Bessen, D. E., Guglielmini, J., Steer, A. C., Carapetis, J. R., Van Melderen, L., Sriprakash, K. S., and Smeesters, P. R. (2013) Updated model of group A Streptococcus M proteins based on a comprehensive worldwide study Clin. Microbiol. Infect. 19, E222-E229
60. Miranda, L. P. and Alewood, P. F. (1999) Accelerated chemical synthesis of peptides and small proteins Proc. Natl. Acad. Sci. U.S.A. 96, 1181-1186