A linear peptide containing minimal T- and B-cell epitopes of Plasmodium falciparum circumsporozoite protein elicits protection against transgenic sporozoite challenge

Infection and Immunity

Volumn 74, Issue 12, 2006, Pages 6929-6939

  Calvo Calle, J Mauricio ^a,c   Oliveira, Giane A ^a,d   Watta, Carol Othoro ^a   Soverow, Jonathan ^a   Parra Lopez, Carlos ^b   Nardin, Elizabeth H ^a  

^a NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b FUNDACIÓN INSTITUTO DE INMUNOLOGÍA DE COLOMBIA FIDIC   (Colombia)

^c UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

^d REGENERON PHARMACEUTICALS INC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADJUVANT; CD4 ANTIGEN; CIRCUMSPOROZOITE PROTEIN; EPITOPE; GAMMA INTERFERON; MALARIA VACCINE; NEUTRALIZING ANTIBODY; PEPTIDE DERIVATIVE; SYNTHETIC PEPTIDE; TETRAPEPTIDE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANTIBODY RESPONSE; ANTIBODY SPECIFICITY; ARTICLE; B LYMPHOCYTE; CD4+ T LYMPHOCYTE; CONTROLLED STUDY; CYTOKINE RELEASE; DRUG EFFICACY; FEMALE; GOLD STANDARD; HIGH RISK POPULATION; IMMUNE RESPONSE; IMMUNIZATION; IMMUNOGENICITY; MALARIA; MORBIDITY; MORTALITY; MOUSE; MOUSE STRAIN; NONHUMAN; PLASMODIUM FALCIPARUM; PRIMATE; PRIORITY JOURNAL; SPOROZOITE; T LYMPHOCYTE; TANDEM REPEAT;

AMINO ACID SEQUENCE; ANIMALS; ANTIBODIES, PROTOZOAN; AOTIDAE; EPITOPES, B-LYMPHOCYTE; EPITOPES, T-LYMPHOCYTE; HUMANS; IMMUNOGLOBULIN G; MALARIA VACCINES; MALARIA, FALCIPARUM; MICE; MOLECULAR SEQUENCE DATA; PEPTIDES; PLASMODIUM FALCIPARUM; SPOROZOITES;

EID: 33845488526     PISSN: 00199567     EISSN: None     Source Type: Journal    
DOI: 10.1128/IAI.01151-06     Document Type: Article

References (67)

1. Alexander, J., J. Sidney, S. Southwood, J. Ruppert, C. Oseroff, A. Maewal, K. Snoke, H. M. Serra, R. T. Kubo, A. Sette, et al. 1994. Development of high potency universal DR-restricted helper epitopes by modification of high affinity DR-blocking peptides. Immunity 1:751-761.
2. Aucouturier, J., L. Dupuis, S. Deville, S. Ascarateil, and V. Ganne. 2002. Montanide ISA 720 and 51: a new generation of water in oil emulsions as adjuvants for human vaccines. Expert Rev. Vaccines 1:111-118.
3. Audran, R., M. Cachat, F. Lurati, S. Soe, O. Leroy, G. Corradin, P. Druilhe, and F. Spertini. 2005. Phase I malaria vaccine trial with a long synthetic peptide derived from the merozoite surface protein 3 antigen. Infect. Immun. 73:8017-8026.
4. Baquero, J. E., S. Miranda, O. Murillo, H. Mateus, E. Trujillo, C. Suarez, M. E. Patarroyo, and C. Parra-Lopez. 2006. Reference strand conformational analysis (RSCA) is a valuable tool in identifying MHC-DRB sequences in three species of Aotus monkeys. Immunogenetics 58:590-597.
5. Bruna-Romero, O., J. C. Hafalla, G. Gonzalez-Aseguinolaza, G. Sano, M. Tsuji, and F. Zavala. 2001. Detection of malaria liver-stages in mice infected through the bite of a single Anopheles mosquito using a highly sensitive real-time PCR. Int. J. Parasitol. 31:1499-1502.
6. Calvo-Calle, J. M., J. Hammer, F. Sinigaglia, P. Clavijo, Z. R. Moya-Castro, and E. H. Nardin. 1997. Binding of malaria T cell epitopes to DR and DQ molecules in vitro correlates with immunogenicity in vivo: identification of a universal T cell epitope in the Plasmodium falciparum circumsporozoite protein. J. Immunol. 159:1362-1373.
7. Calvo-Calle, J. M., G. A. Oliveira, and E. H. Nardin. 2005. Human CD4+ T cells induced by synthetic peptide malaria vaccine are comparable to cells elicited by attenuated Plasmodium falciparum sporozoites. J. Immunol. 175:7575-7585.
8. Cerami, C., U. Frevert, P. Sinnis, B. Takacs, P. Clavijo, M. J. Santos, and V. Nussenzweig. 1992. The basolateral domain of the hepatocyte plasma membrane bears receptors for the circumsporozoite protein of Plasmodium falciparum sporozoites. Cell 70:1021-1033.
9. Chai, S. K., P. Clavijo, J. P. Tam, and F. Zavala. 1992. Immunogenic properties of multiple antigen peptide systems containing defined T and B epitopes. J. Immunol. 149:2385-2390.
10. + T-cell- and gamma interferon-dependent protection against murine malaria by immunization with linear synthetic peptides from a Plasmodium yoelii 17-kilodalton hepatocyte erythrocyte protein. Infect. Immun. 67:5604-5614.
11. Clyde, D. F. 1990. Immunity to falciparum and vivax malaria induced by irradiated sporozoites: a review of the University of Maryland studies, 1971-75. Bull. W. H. O. 68:9-12.
12. Cochrane, A. H., F. Santoro, V. Nussenzweig, R. W. Gwadz, and R. S. Nussenzweig. 1982. Monoclonal antibodies identify the protective antigens of sporozoites of Plasmodium knowlesi. Proc. Natl. Acad. Sci. USA 79:5651-5655.
13. Danforth, H. D., M. Aikawa, A. H. Cochrane, and R. S. Nussenzweig. 1980. Sporozoites of mammalian malaria: attachment to, interiorization and fate within macrophages. J. Protozool. 27:193-202.
14. Del Giudice, G., J. A. Cooper, J. Merino, A. S. Verdini, A. Pessi, A. R. Togna, H. D. Engers, G. Corradin, and P. H. Lambert. 1986. The antibody response in mice to carrier-free synthetic polymers of Plasmodium falciparum circum-sporozoite repetitive epitope is I-Ab-restricted: possible implications for malaria vaccines. J. Immunol. 137:2952-2955.
15. del Guercio, M. F., J. Alexander, R. T. Kubo, T. Arrhenius, A. Maewal, E. Appella, S. L. Hoffman, T. Jones, D. Valmori, K. Sakaguchi, H. M. Grey, and A. Sette. 1997. Potent immunogenic short linear peptide constructs composed of B cell epitopes and Pan DR T helper epitopes (PADRE) for antibody responses in vivo. Vaccine 15:441-448.
16. de Oliveira, G. A., P. Clavijo, R. S. Nussenzweig, and E. H. Nardin. 1994. Immunogenicity of an alum-adsorbed synthetic multiple-antigen peptide based on B- and T-cell epitopes of the Plasmodium falciparum CS protein: possible vaccine application. Vaccine 12:1012-1017.
17. Dhodapkar, M. V., R. M. Steinman, J. Krasovsky, C. Munz, and N. Bhardwaj. 2001. Antigen-specific inhibition of effector T cell function in humans after injection of immature dendritic cells. J. Exp. Med. 193:233-238.
18. Diaz, D., M. Naegeli, R. Rodriguez, J. J. Nino-Vasquez, A. Moreno, M. E. Patarroyo, G. Pluschke, and C. A. Daubenberger. 2000. Sequence and diversity of MHC DQA and DQB genes of the owl monkey Aotus nancymaae. Immunogenetics 51:528-537.
19. Doolan, D. L., and S. L. Hoffman. 2000. The complexity of protective immunity against liver-stage malaria. J. Immunol. 165:1453-1462.
20. Ferreira, A., L. Schofield, V. Enea, H. Schellekens, P. van der Meide, W. E. Collins, R. S. Nussenzweig, and V. Nussenzweig. 1986. Inhibition of development of exoerythrocytic forms of malaria parasites by gamma-interferon. Science 232:881-884.
21. Francis, J. N., and M. Larche. 2005. Peptide-based vaccination: where do we stand? Curr. Opin. Allergy Clin. Immunol. 5:537-543.
22. Franke, E. D., S. L. Hoffman, J. B. Sacci, Jr., R. Wang, Y. Charoenvit, E. Appella, R. Chesnut, J. Alexander, M. F. Del Guercio, and A. Sette. 1999. Pan DR binding sequence provides T-cell help for induction of protective antibodies against Plasmodium yoelii sporozoites. Vaccine 17:1201-1205.
23. Good, M. F., J. A. Berzofsky, W. L. Maloy, Y. Hayashi, N. Fujii, W. T. Hockmeyer, and L. H. Miller. 1986. Genetic control of the immune response in mice to a Plasmodium falciparum sporozoite vaccine. Widespread nonresponsiveness to single malaria T epitope in highly repetitive vaccine. J. Exp. Med. 164:655-660.
24. Gorse, G. J., M. C. Keefer, R. B. Belshe, T. J. Matthews, B. D. Forrest, R. H. Hsieh, W. C. Koff, C. V. Hanson, R. Dolin, K. J. Weinhold, S. E. Frey, N. Ketter, P. E. Fast, and The National Institute of Allergy and Infectious Diseases AIDS Vaccine Evaluation Group. 1996. A dose-ranging study of a prototype synthetic HIV-1MN V3 branched peptide vaccine. J. Infect. Dis. 173:330-339.
25. Herrington, D., J. Davis, E. Nardin, M. Beier, J. Cortese, H. Eddy, G. Losonsky, M. Hollingdale, M. Sztein, M. Levine, et al. 1991. Successful immunization of humans with irradiated malaria sporozoites: humoral and cellular responses of the protected individuals. Am. J. Trop. Med. Hyg. 45:539-547.
26. Herrington, D. A., D. F. Clyde, G. Losonsky, M. Cortesia, J. R. Murphy, J. Davis, S. Baqar, A. M. Felix, E. P. Heimer, D. Gillessen, et al. 1987. Safety and immunogenicity in man of a synthetic peptide malaria vaccine against Plasmodium falciparum sporozoites. Nature 328:257-259.
27. Hoffman, S. L., L. M. Goh, T. C. Luke, I. Schneider, T. P. Le, D. L. Doolan, J. Sacci, P. de la Vega, M. Dowler, C. Paul, D. M. Gordon, J. A. Stoute, L. W. Church, M. Sedegah, D. G. Heppner, W. R. Ballou, and T. L. Richie. 2002. Protection of humans against malaria by immunization with radiation-attenuated Plasmodium falciparum sporozoites. J. Infect. Dis. 185:1155-1164.
28. Klinman, D. M., D. Currie, I. Gursel, and D. Verthelyi. 2004. Use of CpG oligodeoxynucleotides as immune adjuvants. Immunol. Rev. 199:201-216.
29. Kumar, K. A., G. A. Oliveira, R. Edelman, E. Nardin, and V. Nussenzweig. 2004. Quantitative Plasmodium sporozoite neutralization assay (TSNA). J. Immunol. Methods 292:157-164.
30. Lalvani, A., P. Moris, G. Voss, A. A. Pathan, K. E. Kester, R. Brookes, E. Lee, M. Koutsoukos, M. Plebanski, M. Delchambre, K. L. Flanagan, C. Carton, M. Slaoui, C. Van Hoecke, W. R. Ballou, A. V. Hill, and J. Cohen. 1999. Potent induction of focused Th1-type cellular and humoral immune responses by RTS,S/SBAS2, a recombinant Plasmodium falciparum malaria vaccine. J. Infect. Dis. 180:1656-1664.
31. Larche, M., and D. C. Wraith. 2005. Peptide-based therapeutic vaccines for allergic and autoimmune diseases. Nat. Med. 11:S69-S76.
32. Livingston, B. D., C. Crimi, H. Grey, G. Ishioka, F. V. Chisari, J. Fikes, R. W. Chesnut, and A. Sette. 1997. The hepatitis B virus-specific CTL responses induced in humans by lipopeptide vaccination are comparable to those elicited by acute viral infection. J. Immunol. 159:1383-1392.
33. Lopez, J. A., C. Weilenman, R. Audran, M. A. Roggero, A. Bonelo, J. M. Tiercy, F. Spertini, and G. Corradin. 2001. A synthetic malaria vaccine elicits a potent CD8(+) and CD4(+) T lymphocyte immune response in humans. Implications for vaccination strategies. Eur. J. Immunol. 31:1989-1998.
34. Maheshwari, R. K., C. W. Czarniecki, G. P. Dutta, S. K. Puri, B. N. Dhawan, and R. M. Friedman. 1986. Recombinant human gamma interferon inhibits simian malaria. Infect. Immun. 53:628-630.
35. Miyahira, Y., K. Murata, D. Rodriguez, J. R. Rodriguez, M. Esteban, M. M. Rodrigues, and F. Zavala. 1995. Quantification of antigen specific CD8+ T cells using an ELISPOT assay. J. Immunol. Methods 181:45-54.
36. Moreno, A., P. Clavijo, R. Edelman, J. Davis, M. Sztein, F. Sinigaglia, and E. Nardin. 1993. CD4+ T cell clones obtained from Plasmodium falciparum sporozoite-immunized volunteers recognize polymorphic sequences of the circumsporozoite protein. J. Immunol. 151:489-499.
37. Moreno, C. A., R. Rodriguez, G. A. Oliveira, V. Ferreira, R. S. Nussenzweig, Z. R. Moya Castro, J. M. Calvo-Calle, and E. Nardin. 1999. Preclinical evaluation of a synthetic Plasmodium falciparum MAP malaria vaccine in Aotus monkeys and mice. Vaccine 18:89-99.
38. Munesinghe, D. Y., P. Clavijo, M. C. Calle, R. S. Nussenzweig, and E. Nardin. 1991. Immunogenicity of multiple antigen peptides (MAP) containing T and B cell epitopes of the repeat region of the P. falciparum circumsporozoite protein. Eur. J. Immunol. 21:3015-3020.
39. Nardin, E. H., J. M. Calvo-Calle, G. A. Oliveira, P. Clavijo, R. Nussenzweig, R. Simon, W. Zeng, and K. Rose. 1998. 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 16:590-600.
40. Nardin, E. H., J. M. Calvo-Calle, G. A. Oliveira, R. S. Nussenzweig, M. Schneider, J. M. Tiercy, L. Loutan, D. Hochstrasser, and K. Rose. 2001. 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. 166:481-489.
41. Nardin, E. H., D. A. Herrington, J. Davis, M. Levine, D. Stuber, B. Takacs, P. Caspers, P. Barr, R. Altszuler, P. Clavijo, et al. 1989. Conserved repetitive epitope recognized by CD4+ clones from a malaria-immunized volunteer. Science 246:1603-1606.
42. Nardin, E. H., V. Nussenzweig, R. S. Nussenzweig, W. E. Collins, K. T. Harinasuta, P. Tapchaisri, and Y. Chomcharn. 1982. Circumsporozoite proteins of human malaria parasites Plasmodium falciparum and Plasmodium vivax. J. Exp. Med. 156:20-30.
43. Nardin, E. H., G. A. Oliveira, J. M. Calvo-Calle, Z. R. Castro, R. S. Nussenzweig, B. Schmeckpeper, B. F. Hall, C. Diggs, S. Bodison, and R. Edelman. 2000. Synthetic peptide malaria vaccine elicits high levels of antibodies in vaccinees of denned HLA genotypes. J. Infect. Dis. 182:1486-1496.
44. Nino-Vasquez, J. J., D. Vogel, R. Rodriguez, A. Moreno, M. E. Patarroyo, G. Pluschke, and C. A. Daubenberger. 2000. Sequence and diversity of DRB genes of Aotus nancymaae, a primate model for human malaria parasites, Immunogenetics 51:219-230.
45. Nussenzweig, R. S., J. Vanderberg, H. Most, and C. Orton. 1967. Protective immunity produced by the injection of X-irradiated sporozoites of Plasmodium berghei. Nature 216:160-162.
46. Nussenzweig, R. S., J. P. Vanderberg, H. Most, and C. Orton. 1969. Specificity of protective immunity produced by X-irradiated Plasmodium berghei sporozoites. Nature 222:488-489.
47. Nussenzweig, R. S., J. P. Vanderberg, Y. Sanabria, and H. Most. 1972. Plasmodium berghei: accelerated clearance of sporozoites from blood as part of immune-mechanism in mice. Exp. Parasitol. 31:88-97.
48. Nussenzweig, V., and R. S. Nussenzweig. 1989. Rationale for the development of an engineered sporozoite malaria vaccine. Adv. Immunol. 45:283-334.
49. 48a. Kumar, K. A., G.-I. Sano, S. Boscardin, R. S. Nussenzweig, M. C. Nussenzweig, F. Zavala, and V. Nussenzweig. Circumsporozoite protein is an immunodominant protective antigen in irradiated sporozoites. Nature, in press.
50. Persson, C., G. A. Oliveira, A. A. Sultan, P. Bhanot, V. Nussenzweig, and E. Nardin. 2002. Cutting edge: a new tool to evaluate human pre-erythrocytic malaria vaccines: rodent parasites bearing a hybrid Plasmodium falciparum circumsporozoite protein. J. Immunol. 169:6681-6685.
51. Podda, A. 2001. The adjuvanted influenza vaccines with novel adjuvants: experience with the MF59-adjuvanted vaccine. Vaccine 19:2673-2680.
52. Reece, W. H., M. Pinder, P. K. Gothard, P. Milligan, K. Bojang, T. Doherty, M. Plebanski, P. Akinwunmi, S. Everaere, K. R. Watkins, G. Voss, N. Tornieporth, A. Alloueche, B. M. Greenwood, K. E. Kester, K. P. McAdam, J. Cohen, and A. V. Hill. 2004. A CD4(+) T-cell immune response to a conserved epitope in the circumsporozoite protein correlates with protection from natural Plasmodium falciparum infection and disease. Nat. Med. 10:406-410.
53. Romero, P., J. C. Cerottini, and D. E. Speiser. 2004. Monitoring tumor antigen specific T-cell responses in cancer patients and phase I clinical trials of peptide-based vaccination. Cancer Immunol. Immunother. 53:249-255.
54. Schofield, L., A. Ferreira, R. Altszuler, V. Nussenzweig, and R. S. Nussenzweig. 1987. Interferon-gamma inhibits the intrahepatocytic development of malaria parasites in vitro. J. Immunol. 139:2020-2025.
55. Schwenk, R., L. V. Asher, I. Chalom, D. Lanar, P. Sun, K. White, D. Keil, K. E. Kester, J. Stoute, D. G. Heppner, and U. Krzych. 2003. Opsonization by antigen-specific antibodies as a mechanism of protective immunity induced by Plasmodium falciparum circumsporozoite protein-based vaccine. Parasite Immunol. 25:17-25.
56. Snow, R. W., C. A. Guerra, A. M. Noor, H. Y. Myint, and S. I. Hay. 2005. The global distribution of clinical episodes of Plasmodium falciparum malaria. Nature 434:214-217.
57. Steinman, R. M., D. Hawiger, and M. C. Nussenzweig. 2003. Tolerogenic dendritic cells. Annu. Rev. Immunol. 21:685-711.
58. Stewart, M. J., R. J. Nawrot, S. Schulman, and J. P. Vanderberg. 1986. Plasmodium berghei sporozoite invasion is blocked in vitro by sporozoite-immobilizing antibodies. Infect. Immun. 51:859-864.
59. Stoute, J. A., M. Slaoui, D. G. Heppner, P. Momin, K. E. Kester, P. Desmons, B. T. Wellde, N. Garçon, U. Krzych, M. Marchand, W. R. Ballou, and J. D. Cohen for the RTS,S Malaria Vaccine Evaluation Group. 1997. A preliminary evaluation of a recombinant circumsporozoite protein vaccine against Plasmodium falciparum malaria. RTS,S Malaria Vaccine Evaluation Group. N. Engl. J. Med. 336:86-91.
60. Sultan, A. A., V. Thathy, U. Frevert, K. J. Robson, A. Crisanti, V. Nussenzweig, R. S. Nussenzweig, and R. Menard. 1997. TRAP is necessary for gliding motility and infectivity of plasmodium sporozoites. Cell 90:511-522.
61. Sun, P., R. Schwenk, K. White, J. A. Stoute, J. Cohen, W. R. Ballou, G. Voss, K. E. Kester, D. G. Heppner, and U. Krzych. 2003. Protective immunity induced with malaria vaccine, RTS,S, is linked to Plasmodium falciparum circumsporozoite protein-specific CD4+ and CD8+ T cells producing IFN-gamma. J. Immunol. 171:6961-6967.
62. Tam, J. P., P. Clavijo, Y. A. Lu, V. Nussenzweig, R. Nussenzweig, and F. Zavala. 1990. Incorporation of T and B epitopes of the circumsporozoite protein in a chemically defined synthetic vaccine against malaria. J Exp. Med. 171:299-306.
63. Vanderberg, J. P., and U. Frevert. 2004. Intravital microscopy demonstrating antibody-mediated immobilisation of Plasmodium berghei sporozoites injected into skin by mosquitoes. Int. J. Parasitol. 34:991-996.
64. Wang, R., Y. Charoenvit, G. Corradin, P. De La Vega, E. D. Franke, and S. L. Hoffman. 1996. Protection against malaria by Plasmodium yoelii sporozoite surface protein 2 linear peptide induction of CD4+ T cell- and IFN-gamma-dependent elimination of infected hepatocytes. J. Immunol. 157:4061-4067.
65. Wang, R., Y. Charoenvit, G. Corradin, R. Porrozzi, R. L. Hunter, G. Glenn, C. R. Alving, P. Church, and S. L. Hoffman. 1995. Induction of protective polyclonal antibodies by immunization with a Plasmodium yoelii circumsporozoite protein multiple antigen peptide vaccine. J. Immunol. 154:2784-2793. (Erratum, 155:1637.)
66. White, K. L., H. L. Snyder, and U. Krzych. 1996. MHC class I-dependent presentation of exoerythrocytic antigens to CD8+ T lymphocytes is required for protective immunity against Plasmodium berghei. J. Immunol. 156:3374-3381.
67. Zavala, F., J. P. Tam, P. J. Barr, P. J. Romero, V. Ley, R. S. Nussenzweig, and V. Nussenzweig. 1987. Synthetic peptide vaccine confers protection against murine malaria. J. Exp. Med. 166:1591-1596.