Self-assembled peptide nanofibers raising durable antibody responses against a malaria epitope

Biomaterials

Volumn 33, Issue 27, 2012, Pages 6476-6484

  Rudra, Jai S ^a   Mishra, Satish ^b   Chong, Anita S ^a   Mitchell, Robert A ^b   Nardin, Elizabeth H ^b   Nussenzweig, Victor ^b   Collier, Joel H ^a  

^a UNIVERSITY OF CHICAGO   (United States)

^b NEW YORK UNIVERSITY   (United States)

Author keywords

Immune response; Immunomodulation; Immunostimulation; Peptide; Self assembly

Indexed keywords

ADAPTIVE IMMUNE RESPONSE; ANTIBODY RESPONSE; ANTIBODY TITERS; C57BL/6 MICE; IMMUNE RESPONSE; IMMUNOGENICITY; IMMUNOMODULATION; IMMUNOSTIMULATION; KNOCKOUT MICE; PEPTIDE EPITOPES; PLASMODIUM FALCIPARUM; SELF-ASSEMBLED; SELF-ASSEMBLED PEPTIDES; SELF-ASSEMBLING; SELF-ASSEMBLING PEPTIDES; SYNTHETIC PEPTIDE; T CELLS; TRANSGENICS;

ANTIGENS; ASSAYS; DISEASES; ENZYME ACTIVITY; IMMUNOLOGY; MAMMALS; NANOFIBERS; PEPTIDES; SELF ASSEMBLY; STRENGTH OF MATERIALS;

ANTIBODIES;

(NANP) 3 Q11 PEPTIDE; CIRCUMSPOROZOITE PROTEIN; EPITOPE; MYELOID DIFFERENTIATION FACTOR 88; NANOFIBER; NEUTRALIZING ANTIBODY; PEPTIDE DERIVATIVE; TOLL LIKE RECEPTOR 5; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIBODY RESPONSE; ANTIBODY TITER; ANTIGEN ANTIBODY REACTION; ARTICLE; CONTROLLED STUDY; FEMALE; IMMUNOGENICITY; IRRADIATION; KNOCKOUT MOUSE; MALARIA; MOUSE; NONHUMAN; PLASMODIUM FALCIPARUM; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN DOMAIN; PROTEIN FUNCTION; SPOROZOITE; T LYMPHOCYTE;

AMINO ACID SEQUENCE; ANIMALS; ANTIBODIES, PROTOZOAN; ANTIBODY FORMATION; ENZYME-LINKED IMMUNOSORBENT ASSAY; EPITOPES; MALARIA; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MOLECULAR SEQUENCE DATA; MYELOID DIFFERENTIATION FACTOR 88; NANOFIBERS; OLIGOPEPTIDES; PEPTIDES; PROTEIN STRUCTURE, SECONDARY; SPOROZOITES; T-LYMPHOCYTES;

MUS; PLASMODIUM FALCIPARUM;

EID: 84863568613     PISSN: 01429612     EISSN: 18785905     Source Type: Journal    
DOI: 10.1016/j.biomaterials.2012.05.041     Document Type: Article

References (60)

1. Purcell A.W., McCluskey J., Rossjohn J. More than one reason to rethink the use of peptides in vaccine design. Nat Rev Drug Discov 2007, 6:404-414.
2. Black M., Trent A., Tirrell M., Olive C. Advances in the design and delivery of peptide subunit vaccines with a focus on toll-like receptor agonists. Expert Rev Vaccines 2010, 9:157-173.
3. Corradin G., Kajava A.V., Verdini A. Long synthetic peptides for the production of vaccines and drugs: a technological platform coming of age. Sci Transl Med 2010, 2:50rv3.
4. Coffman R.L., Sher A., Seder R.A. Vaccine adjuvants: putting innate immunity to work. Immunity 2010, 33:492-503.
5. O'Hagan D.T., De Gregorio E. The path to a successful vaccine adjuvant-the long and winding road. Drug Discov Today 2009, 14:541-551.
6. Rudra J.S., Tian Y.F., Jung J.P., Collier J.H. A self-assembling peptide acting as an immune adjuvant. Proc Natl Acad Sci U S A 2010, 107:622-627.
7. Kaltgrad E., Sen Gupta S., Punna S., Huang C.Y., Chang A., Wong C.H., et al. Anti-carbohydrate antibodies elicited by polyvalent display on a viral scaffold. Chembiochem 2007, 8:1455-1462.
8. Kaba S.A., Brando C., Guo Q., Mittelholzer C., Raman S., Tropel D., et al. A nonadjuvanted polypeptide nanoparticle vaccine confers long-lasting protection against rodent malaria. J Immunol 2009, 183:7268-7277.
9. Schroeder U., Graff A., Buchmeier S., Rigler P., Silvan U., Tropel D., et al. Peptide nanoparticles serve as a powerful platform for the immunogenic display of poorly antigenic actin determinants. J Mol Biol 2009, 386:1368-1381.
10. Boato F., Thomas R.M., Ghasparian A., Freund-Renard A., Moehle K., Robinson J.A. Synthetic virus-like particles from self-assembling coiled-coil lipopeptides and their use in antigen display to the immune system. Angew Chem Int Ed 2007, 46:9015-9018.
11. 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.
12. Riedel T., Ghasparian A., Moehle K., Rusert P., Trkola A., Robinson J.A. Synthetic virus-like particles and conformationally constrained peptidomimetics in vaccine design. Chembiochem 2011, 12:2829-2836.
13. Braun M., Jandus C., Maurer P., Hammann-Haenni A., Schwarz K., Bachmann M.F., et al. Virus-like particles induce robust human T-helper cell responses. Eur J Immunol 2012, 42:330-340.
14. Toth I., Simerska P., Fujita Y. Recent advances in design and synthesis of self-adjuvanting lipopeptide vaccines. Int J Pept Res Ther 2008, 14:333-340.
15. 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.
16. Chackerian B., Durfee M.R., Schiller J.T. Virus-like display of a neo-self antigen reverses B cell anergy in a B cell receptor transgenic mouse model. J Immunol 2008, 180:5816-5825.
17. Jung J.P., Nagaraj A.K., Fox E.K., Rudra J.S., Devgun J.M., Collier J.H. Co-assembling peptides as defined matrices for endothelial cells. Biomaterials 2009, 30:2400-2410.
18. Jung J.P., Jones J.L., Cronier S.A., Collier J.H. Modulating the mechanical properties of self-assembled peptide hydrogels via native chemical ligation. Biomaterials 2008, 29:2143-2151.
19. Jung J.P., Moyano J.V., Collier J.H. Multifactorial optimization of endothelial cell growth using modular synthetic extracellular matrices. Integr Biol 2011, 3:185-196.
20. Rudra J.S., Sun T., Bird K.C., Daniels M.D., Gasiorowski J.Z., Chong A.S., et al. Modulating adaptive immune responses to peptide self-assemblies. ACS Nano 2012, 6:1557-1564.
21. Mbow M.L., De Gregorio E., Valiante N.M., Rappuoli R. New adjuvants for human vaccines. Curr Opin Immunol 2010, 22:411-416.
22. Hubbell J.A., Thomas S.N., Swartz M.A. Materials engineering for immunomodulation. Nature 2009, 462:449-460.
23. Kim J., Mooney D.J. In vivo modulation of dendritic cells by engineered materials: towards new cancer vaccines. Nano Today 2011, 6:466-477.
24. Pulendran B. Modulating vaccine responses with dendritic cells and toll-like receptors. Immunol Rev 2004, 199:227-250.
25. Salazar-Gonzalez R.M., McSorley S.J. Salmonella flagellin, a microbial target of the innate and adaptive immune system. Immunol Lett 2005, 101:117-122.
26. Tukel C., Nishimori J.H., Wilson R.P., Winter M.G., Keestra A.M., van Putten J.P., et al. Toll-like receptors 1 and 2 cooperatively mediate immune responses to curli, a common amyloid from enterobacterial biofilms. Cell Microbiol 2010, 12:1495-1505.
27. Eisenbarth S.C., Colegio O.R., O'Connor W., Sutterwala F.S., Flavell R.A. Crucial role for the Nalp3 inflammasome in the immunostimulatory properties of aluminium adjuvants. Nature 2008, 453:1122-1126.
28. Nardin E.H. The past decade in malaria synthetic peptide vaccine clinical trials. Hum Vaccin 2010, 6:27-38.
29. Kumar K.A., Sano G., Boscardin S., Nussenzweig R.S., Nussenzweig M.C., Zavala F., et al. The circumsporozoite protein is an immunodominant protective antigen in irradiated sporozoites. Nature 2006, 444:937-940.
30. Nussenzweig V., Nussenzweig R.S. Rationale for the development of an engineered sporozoite malaria vaccine. Adv Immunol 1989, 45:283-334.
31. Lopez J.A., Weilenman C., Audran R., Roggero M.A., Bonelo A., Tiercy J.M., et al. A synthetic malaria vaccine elicits a potent CD8(+) and CD4(+) T lymphocyte immune response in humans. Implications vaccination strategies. Eur J Immunol 2001, 31:1989-1998.
32. Nardin E.H., Oliveira G.A., Calvo-Calle J.M., Castro Z.R., Nussenzweig R.S., Schmeckpeper B., et al. Synthetic malaria peptide vaccine elicits high levels of antibodies in vaccinees of defined HLA genotypes. J Infect Dis 2000, 182:1486-1496.
33. Nardin E.H., Calvo-Calle J.M., Oliveira G.A., Nussenzweig R.S., Schneider M., Tiercy J.M., et al. A totally synthetic polyoxime malaria vaccine containing Plasmodium falciparum B cell and universal T cell epitopes elicits immune responses in volunteers of diverse HLA types. J Immunol 2001, 166:481-489.
34. Alonso P.L., Sacarlal J., Aponte J.J., Leach A., Macete E., Milman J., et al. Efficacy of the RTS, S/AS02A vaccine against Plasmodium falciparum infection and disease in young african children: randomised controlled trial. Lancet 2004, 364:1411-1420.
35. Hollingdale M.R., Nardin E.H., Tharavanij S., Schwartz A.L., Nussenzweig R.S. Inhibition of entry of Plasmodium falciparum and Plasmodium vivax sporozoites into cultured cells - an in vitro assay of protective antibodies. J Immunol 1984, 132:909-913.
36. Kumar K.A., Oliveira G.A., Edelman R., Nardin E.H., Nussenzweig V. Quantitative plasmodium sporozoite neutralization assay (TSNA). J Immunol Methods 2004, 292:157-164.
37. Othoro C., Johnston D., Lee R., Soverow J., Bystryn J.C., Nardin E.H. Enhanced immunogenicity of plasmodium falciparum peptide vaccines using a topical adjuvant containing a potent synthetic toll-like receptor 7 agonist, imiquimod. Infect Immun 2009, 77:739-748.
38. Malyala P., Singh M. Endotoxin limits in formulations for preclinical research. J Pharm Sci 2008, 97:2043-2046.
39. Nardin E.H., Calvo-Calle J.M., Oliveira G.A., Clavijo P., Nussenzweig R., Simon R., et al. Plasmodium falciparum polyoximes: highly immunogenic synthetic vaccines constructed by chemoselective ligation of repeat B-cell epitopes and a universal T-cell epitope of CS protein. Vaccine 1998, 16:590-600.
40. Oliveira G.A., Clavijo P., Nussenzweig R.S., Nardin E.H. Immunogenicity of an alum-adsorbed synthetic multiple-antigen peptide-based on B-cell and T-cell epitopes of the Plasmodium falciparum CS protein - possible vaccine application. Vaccine 1994, 12:1012-1017.
41. Persson C., Oliveira G.A., Sultan A.A., Bhanot P., Nussenzweig V., Nardin E.H. Cutting edge: a new tool to evaluate human pre-erythrocytic malaria vaccines: rodent parasites bearing a hybrid Plasmodium falciparum circumsporozoite protein. J Immunol 2002, 169:6681-6685.
42. Lambrecht B.N., Kool M., Willart M.A.M., Hammad H. Mechanism of action of clinically approved adjuvants. Curr Opin Immunol 2009, 21:23-29.
43. Marrack P., McKee A.S., Munks M.W. Towards an understanding of the adjuvant action of aluminium. Nat Rev Immunol 2009, 9:287-293.
44. Mellinkoff S.M., Pearson C.M., Wood F.D., Eshelmano Dixon W. Studies of polyarthritis induced in rats by injection of mycobacterial adjuvant. VI. Effects of dietary alterations. Am J Clin Nutr 1962, 10:398-402.
45. Good M.F., Berzofsky J.A., Maloy W.L., Hayashi Y., Fujii N., Hockmeyer W.T., et al. Genetic control of the immune response in mice to a Plasmodium falciparum sporozoite vaccine. Widespread nonresponsiveness to a single malaria T epitope in highly repetitive vaccine. J Exp Med 1986, 164:655-660.
46. b-restricted: possible implications for malaria vaccines. J Immunol 1986, 137:2952-2955.
47. Ahlers J.D., Belyakov I.M. Molecular pathways regulating CD4(+) T cell differentiation, anergy and memory with implications for vaccines. Trends Mol Med 2010, 16:478-491.
48. Jones K.S. Biomaterials as vaccine adjuvants. Biotechnol Prog 2008, 24:807-814.
49. Demento S.L., Siefert A.L., Bandyopadhyay A., Sharp F.A., Fahmy T.M. Pathogen-associated molecular patterns on biomaterials: a paradigm for engineering new vaccines. Trends Biotechnol 2011, 29:294-306.
50. Kou P.M., Babensee J.E. Macrophage and dendritic cell phenotypic diversity in the context of biomaterials. J Biomed Mater Res A 2011, 96:239-260.
51. Yoshida M., Mata J., Babensee J.E. Effect of poly(lactic-co-glycolic acid) contact on maturation of murine bone marrow-derived dendritic cells. J Biomed Mater Res A 2007, 80A:7-12.
52. Yang D., Jones K.S. Effect of alginate on innate immune activation of macrophages. J Biomed Mater Res A 2009, 90:411-418.
53. Nussenzweig R.S., Vanderberg J., Most H., Orton C. Protective immunity produced by injection of x-irradiated sporozoites of Plasmodium berghei. Nature 1967, 216:160-162.
54. Herrington D., Davis J., Nardin E.H., Beier M., Cortese J., Eddy H., et al. Successful immunization of humans with irradiated malaria sporozoites - humoral and cellular responses of the protected individuals. Am J Trop Med Hyg 1991, 45:539-547.
55. Hoffman S.L., Goh L.M.L., Luke T.C., Schneider I., Le T.P., Doolan D.L., et al. Protection of humans against malaria by immunization with radiation-attenuated Plasmodium falciparum sporozoites. J Infect Dis 2002, 185:1155-1164.
56. Moreno C.A., Rodriguez R., Oliveira G.A., Ferreira V., Nussenzweig R.S., Castro Z.R.M., et al. Preclinical evaluation of a synthetic Plasmodium falciparum MAP malaria vaccine in aotus monkeys and mice. Vaccine 1999, 18:89-99.
57. Matzelle M.M., Babensee J.E. Humoral immune responses to model antigen co-delivered with biomaterials used in tissue engineering. Biomaterials 2004, 25:295-304.
58. Carcaboso A.M., Hernandez R.M., Igartua M., Rosas J.E., Patarroyo M.E., Pedraz J.L. Enhancing immunogenicity and reducing dose of microparticulated synthetic vaccines: single intradermal administration. Pharm Res 2004, 21:121-126.
59. De Koker S., Lambrecht B.N., Willart M.A., van Kooyk Y., Grooten J., Vervaet C., et al. Designing polymeric particles for antigen delivery. Chem Soc Rev 2011, 40:320-339.
60. Schwendeman S.P., Costantino H.R., Gupta R.K., Siber G.R., Klibanov A.M., Langer R. Stabilization of tetanus and diphtheria toxoids against moisture-induced aggregation. Proc Natl Acad Sci U S A 1995, 92:11234-11238.