Immunogenic properties of a recombinant fusion protein containing the C-terminal 19 kDa of Plasmodium falciparum merozoite surface protein-1 and the innate immunity agonist FliC flagellin of Salmonella Typhimurium

Vaccine

Volumn 28, Issue 16, 2010, Pages 2818-2826

  Bargieri, Daniel Y ^a   Leite, Juliana A ^b   Lopes, Stefanie C P ^b   Sbrogio Almeida, Maria Elisabete ^c   Braga, Catarina J M ^d   Ferreira, Luis C S ^d   Soares, Irene S ^e   Costa, Fabio T M ^b   Rodrigues, Mauricio M ^a  

^a FEDERAL UNIVERSITY OF SÃO PAULO   (Brazil)

^b UNIVERSITY OF CAMPINAS   (Brazil)

^c INSTITUTO BUTANTAN   (Brazil)

^d UNIVERSITY OF SÃO PAULO   (Brazil)

^e Faculdade de Ciencias Farmaceuticas   (Brazil)

Author keywords

Flagellin; P. falciparum; TLR5; Vaccine

Indexed keywords

CPG OLIGODEOXYNUCLEOTIDE; FLAGELLIN MEROZOITE SURFACE PROTEIN 1 FUSION PROTEIN; FREUND ADJUVANT; GAMMA INTERFERON; IMMUNOGLOBULIN G ANTIBODY; IMMUNOGLOBULIN G2; MALARIA VACCINE; QUIL A; TOLL LIKE RECEPTOR 5; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIBODY RESPONSE; ANTIBODY TITER; ANTIGEN SPECIFICITY; ARTICLE; CELLULAR IMMUNITY; CONTROLLED STUDY; ENZYME LINKED IMMUNOSORBENT ASSAY; ESCHERICHIA COLI; FEMALE; IMMUNE RESPONSE; IMMUNIZATION; IMMUNOFLUORESCENCE; IMMUNOGENICITY; IN VITRO STUDY; INNATE IMMUNITY; MALARIA; MOUSE; NONHUMAN; PLASMODIUM FALCIPARUM; PRIORITY JOURNAL; PROTEIN EXPRESSION; RABBIT; SALMONELLA ENTERICA; SALMONELLA TYPHIMURIUM; SPLEEN CELL;

ADJUVANTS, IMMUNOLOGIC; ANIMALS; ANTIBODIES, PROTOZOAN; BACTERIAL PROTEINS; ESCHERICHIA COLI; FEMALE; FLAGELLIN; GENE EXPRESSION; IMMUNOGLOBULIN G; INJECTIONS, SUBCUTANEOUS; INTERFERON-GAMMA; LEUKOCYTES, MONONUCLEAR; MALARIA VACCINES; MEROZOITE SURFACE PROTEIN 1; MICE; MICE, INBRED C57BL; PLASMODIUM FALCIPARUM; RECOMBINANT FUSION PROTEINS; SALMONELLA TYPHIMURIUM; SPLEEN; VACCINES, SYNTHETIC;

EID: 77949658432     PISSN: 0264410X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.vaccine.2010.02.004     Document Type: Article

References (63)

1. Aregawi M., Cibulskis R., Otten M., Williams R., and Dye C. World malaria report 2008 (2008), World Health Organization (WHO)
2. White N.J. Antimalarial drug resistance. J Clin Invest 113 April (8) (2004) 1084-1092
3. Beeson J.G., Osier F.H., and Engwerda C.R. Recent insights into humoral and cellular immune responses against malaria. Trends Parasitol 24 December (12) (2008) 578-584
4. Yazdani S.S., Mukherjee P., Chauhan V.S., and Chitnis C.E. Immune responses to asexual blood-stages of malaria parasites. Curr Mol Med 6 March (2) (2006) 187-203
5. Doolan D.L., and Martinez-Alier N. Immune response to pre-erythrocytic stages of malaria parasites. Curr Mol Med 6 March (2) (2006) 169-185
6. Renia L. Protective immunity against malaria liver stage after vaccination with live parasites. Parasite (Paris, France) 15 September (3) (2008) 379-383
7. Bejon P., Lusingu J., Olotu A., Leach A., Lievens M., Vekemans J., et al. Efficacy of RTS,S/AS01E vaccine against malaria in children 5 to 17 months of age. N Engl J Med 359 December (24) (2008) 2521-2532
8. Abdulla S., Oberholzer R., Juma O., Kubhoja S., Machera F., Membi C., et al. Safety and immunogenicity of RTS,S/AS02D malaria vaccine in infants. N Engl J Med 359 December (24) (2008) 2533-2544
9. Diggs C.L., Ballou W.R., and Miller L.H. The major merozoite surface protein as a malaria vaccine target. Parasitol Today 9 August (8) (1993) 300-302 [Personal ed]
10. Blackman M.J., Heidrich H.G., Donachie S., McBride J.S., and Holder A.A. A single fragment of a malaria merozoite surface protein remains on the parasite during red cell invasion and is the target of invasion-inhibiting antibodies. J Exp Med 172 July (1) (1990) 379-382
11. O'Donnell R.A., Saul A., Cowman A.F., and Crabb B.S. Functional conservation of the malaria vaccine antigen MSP-119 across distantly related Plasmodium species. Nat Med 6 January (1) (2000) 91-95
12. Combe A., Giovannini D., Carvalho T.G., Spath S., Boisson B., Loussert C., et al. Clonal conditional mutagenesis in malaria parasites. Cell Host Microbe 5 April (4) (2009) 386-396
13. Bergmann-Leitner E.S., Duncan E.H., and Angov E. MSP-1p42-specific antibodies impact growth and development of intra-erythrocytic parasites of Plasmodium falciparum. Malar J 8 August (1) (2009) 183
14. Chang S.P., Case S.E., Gosnell W.L., Hashimoto A., Kramer K.J., Tam L.Q., et al. A recombinant baculovirus 42-kilodalton C-terminal fragment of Plasmodium falciparum merozoite surface protein 1 protects Aotus monkeys against malaria. Infect Immun 64 January (1) (1996) 253-261
15. Stowers A.W., Cioce V., Shimp R.L., Lawson M., Hui G., Muratova O., et al. Efficacy of two alternate vaccines based on Plasmodium falciparum merozoite surface protein 1 in an Aotus challenge trial. Infect Immun 69 March (3) (2001) 1536-1546
16. Lyon J.A., Angov E., Fay M.P., Sullivan J.S., Girourd A.S., Robinson S.J., et al. Protection induced by Plasmodium falciparum MSP1(42) is strain-specific, antigen and adjuvant dependent, and correlates with antibody responses. PLoS One 3 7 (2008) e2830
17. Kumar S., Yadava A., Keister D.B., Tian J.H., Ohl M., Perdue-Greenfield K.A., et al. Immunogenicity and in vivo efficacy of recombinant Plasmodium falciparum merozoite surface protein-1 in Aotus monkeys. Mol Med (Cambridge, MA) 1 March (3) (1995) 325-332
18. Singh S., Miura K., Zhou H., Muratova O., Keegan B., Miles A., et al. Immunity to recombinant Plasmodium falciparum merozoite surface protein 1 (MSP1): protection in Aotus nancymai monkeys strongly correlates with anti-MSP1 antibody titer and in vitro parasite-inhibitory activity. Infect Immun 74 August (8) (2006) 4573-4580
19. Darko C.A., Angov E., Collins W.E., Bergmann-Leitner E.S., Girouard A.S., Hitt S.L., et al. The clinical-grade 42-kilodalton fragment of merozoite surface protein 1 of Plasmodium falciparum strain FVO expressed in Escherichia coli protects Aotus nancymai against challenge with homologous erythrocytic-stage parasites. Infect Immun 73 January (1) (2005) 287-297
20. Stowers A.W., Chen Lh L.H., Zhang Y., Kennedy M.C., Zou L., Lambert L., et al. A recombinant vaccine expressed in the milk of transgenic mice protects Aotus monkeys from a lethal challenge with Plasmodium falciparum. Proc Natl Acad Sci USA 99 January (1) (2002) 339-344
21. Janeway Jr. C.A., and Medzhitov R. Innate immune recognition. Annu Rev Immunol 20 (2002) 197-216
22. Akira S., Uematsu S., and Takeuchi O. Pathogen recognition and innate immunity. Cell 124 February (4) (2006) 783-801
23. Miao E.A., Alpuche-Aranda C.M., Dors M., Clark A.E., Bader M.W., Miller S.I., et al. Cytoplasmic flagellin activates caspase-1 and secretion of interleukin 1beta via Ipaf. Nat Immunol 7 June (6) (2006) 569-575
24. Smith K.D., Andersen-Nissen E., Hayashi F., Strobe K., Bergman M.A., Barrett S.L., et al. Toll-like receptor 5 recognizes a conserved site on flagellin required for protofilament formation and bacterial motility. Nat Immunol 4 December (12) (2003) 1247-1253
25. Franchi L., Amer A., Body-Malapel M., Kanneganti T.D., Ozoren N., Jagirdar R., et al. Cytosolic flagellin requires Ipaf for activation of caspase-1 and interleukin 1beta in salmonella-infected macrophages. Nat Immunol 7 June (6) (2006) 576-582
26. Lamkanfi M., Amer A., Kanneganti T.D., Munoz-Planillo R., Chen G., Vandenabeele P., et al. The Nod-like receptor family member Naip5/Birc1e restricts Legionella pneumophila growth independently of caspase-1 activation. J Immunol 178 June (12) (2007) 8022-8027
27. Zamboni D.S., Kobayashi K.S., Kohlsdorf T., Ogura Y., Long E.M., Vance R.E., et al. The Birc1e cytosolic pattern-recognition receptor contributes to the detection and control of Legionella pneumophila infection. Nat Immunol 7 March (3) (2006) 318-325
28. Vinzing M., Eitel J., Lippmann J., Hocke A.C., Zahlten J., Slevogt H., et al. NAIP and Ipaf control Legionella pneumophila replication in human cells. J Immunol 180 May (10) (2008) 6808-6815
29. Ren T., Zamboni D.S., Roy C.R., Dietrich W.F., and Vance R.E. Flagellin-deficient Legionella mutants evade caspase-1- and Naip5-mediated macrophage immunity. PLoS Pathog 2 March (3) (2006) e18
30. Hayashi F., Smith K.D., Ozinsky A., Hawn T.R., Yi E.C., Goodlett D.R., et al. The innate immune response to bacterial flagellin is mediated by Toll-like receptor 5. Nature 410 April (6832) (2001) 1099-1103
31. McDonald W.F., Huleatt J.W., Foellmer H.G., Hewitt D., Tang J., Desai P., et al. A West Nile virus recombinant protein vaccine that coactivates innate and adaptive immunity. J Infect Dis 195 June (11) (2007) 1607-1617
32. Ben-Yedidia T., Tarrab-Hazdai R., Schechtman D., and Arnon R. Intranasal administration of synthetic recombinant peptide-based vaccine protects mice from infection by Schistosoma mansoni. Infect Immun 67 September (9) (1999) 4360-4366
33. Cuadros C., Lopez-Hernandez F.J., Dominguez A.L., McClelland M., and Lustgarten J. Flagellin fusion proteins as adjuvants or vaccines induce specific immune responses. Infect Immun 72 May (5) (2004) 2810-2816
34. Chauhan N., Kumar R., Badhai J., Preet A., and Yadava P.K. Immunogenicity of cholera toxin B epitope inserted in Salmonella flagellin expressed on bacteria and administered as DNA vaccine. Mol Cell Biochem 276 August (1-2) (2005) 1-6
35. Huleatt J.W., Jacobs A.R., Tang J., Desai P., Kopp E.B., Huang Y., et al. Vaccination with recombinant fusion proteins incorporating Toll-like receptor ligands induces rapid cellular and humoral immunity. Vaccine 25 January (4) (2007) 763-775
36. Huleatt J.W., Nakaar V., Desai P., Huang Y., Hewitt D., Jacobs A., et al. Potent immunogenicity and efficacy of a universal influenza vaccine candidate comprising a recombinant fusion protein linking influenza M2e to the TLR5 ligand flagellin. Vaccine 26 January (2) (2008) 201-214
37. Song L., Nakaar V., Kavita U., Price A., Huleatt J., Tang J., et al. Efficacious recombinant influenza vaccines produced by high yield bacterial expression: a solution to global pandemic and seasonal needs. PLoS One 3 5 (2008) e2257
38. Adar Y., Singer Y., Levi R., Tzehoval E., Perk S., Banet-Noach C., et al. A universal epitope-based influenza vaccine and its efficacy against H5N1. Vaccine 27 March (15) (2009) 2099-2107
39. Le Moigne V., Robreau G., and Mahana W. Flagellin as a good carrier and potent adjuvant for Th1 response: study of mice immune response to the p27 (Rv2108) Mycobacterium tuberculosis antigen. Mol Immunol 45 May (9) (2008) 2499-2507
40. Braga C.J., Rittner G.M., Munoz Henao J.E., Teixeira A.F., Massis L.M., Sbrogio-Almeida M.E., et al. Paracoccidioides brasiliensis vaccine formulations based on the gp43-derived P10 sequence and the Salmonella enterica FliC flagellin. Infect Immun 77 April (4) (2009) 1700-1707
41. Lee S.E., Kim S.Y., Jeong B.C., Kim Y.R., Bae S.J., Ahn O.S., et al. A bacterial flagellin, Vibrio vulnificus FlaB, has a strong mucosal adjuvant activity to induce protective immunity. Infect Immun 74 January (1) (2006) 694-702
42. Pino O., Martin M., and Michalek S.M. Cellular mechanisms of the adjuvant activity of the flagellin component FljB of Salmonella enterica serovar Typhimurium to potentiate mucosal and systemic responses. Infect Immun 73 October (10) (2005) 6763-6770
43. Honko A.N., Sriranganathan N., Lees C.J., and Mizel S.B. Flagellin is an effective adjuvant for immunization against lethal respiratory challenge with Yersinia pestis. Infect Immun 74 February (2) (2006) 1113-1120
44. Mizel S.B., Graff A.H., Sriranganathan N., Ervin S., Lees C.J., Lively M.O., et al. Flagellin-F1-V fusion protein is an effective plague vaccine in mice and two species of nonhuman primates. Clin Vaccine Immunol 16 1 (2009 Jan) 21-28
45. Weimer E.T., Lu H., Kock N.D., Wozniak D.J., and Mizel S.B. A fusion protein vaccine containing OprF epitope 8, OprI, and type A and B flagellins promotes enhanced clearance of nonmucoid Pseudomonas aeruginosa. Infect Immun 77 June (6) (2009) 2356-2366
46. Bargieri D.Y., Rosa D.S., Braga C.J., Carvalho B.O., Costa F.T., Espindola N.M., et al. New malaria vaccine candidates based on the Plasmodium vivax merozoite surface protein-1 and the TLR-5 agonist Salmonella Typhimurium FliC flagellin. Vaccine 26 November (48) (2008) 6132-6142
47. Cunha M.G., Rodrigues M.M., and Soares I.S. Comparison of the immunogenic properties of recombinant proteins representing the Plasmodium vivax vaccine candidate MSP1(19) expressed in distinct bacterial vectors. Vaccine 20 November (3-4) (2001) 385-396
48. Schmitt C.K., Darnell S.C., and O'Brien A.D. The attenuated phenotype of a Salmonella typhimurium flgM mutant is related to expression of FliC flagellin. J Bacteriol 178 May (10) (1996) 2911-2915
49. Rodrigues M.M., Ribeirao M., Pereira-Chioccola V., Renia L., and Costa F. Predominance of CD4 Th1 and CD8 Tc1 cells revealed by characterization of the cellular immune response generated by immunization with a DNA vaccine containing a Trypanosoma cruzi gene. Infect Immun 67 August (8) (1999) 3855-3863
50. Lekana Douki J.B., Traore B., Costa F.T., Fusai T., Pouvelle B., Sterkers Y., et al. Sequestration of Plasmodium falciparum-infected erythrocytes to chondroitin sulfate A, a receptor for maternal malaria: monoclonal antibodies against the native parasite ligand reveal pan-reactive epitopes in placental isolates. Blood 100 August (4) (2002) 1478-1483
51. di Santi S.M., Boulos M., Vasconcelos M.A., Oliveira S., Couto A., and Rosario V.E. Characterization of Plasmodium falciparum strains of the State of Rondonia, Brazil, using microtests of sensitivity to antimalarials, enzyme typing and monoclonal antibodies. Rev Inst Med Trop Sao Paulo 29 May-June (3) (1987) 142-147
52. Trager W., and Jensen J.B. Human malaria parasites in continuous culture. Science (New York, NY) 193 August (4254) (1976) 673-675
53. Ljungström I., Perlmann H., Schlichtherle M., Scherf A., and Wahlgren M. Methods in malaria research. 4th ed. (2004) [Manassas, Virginia, USA: MR4/ATCC]
54. Kulane A., Ekre H.P., Perlmann P., Rombo L., Wahlgren M., and Wahlin B. Effect of different fractions of heparin on Plasmodium falciparum merozoite invasion of red blood cells in vitro. Am J Trop Med Hygiene 46 May (5) (1992) 589-594
55. O'Donnell R.A., de Koning-Ward T.F., Burt R.A., Bockarie M., Reeder J.C., Cowman A.F., et al. Antibodies against merozoite surface protein (MSP)-1(19) are a major component of the invasion-inhibitory response in individuals immune to malaria. J Exp Med 193 June (12) (2001) 1403-1412
56. Ogutu B.R., Apollo O.J., McKinney D., Okoth W., Siangla J., Dubovsky F., et al. Blood stage malaria vaccine eliciting high antigen-specific antibody concentrations confers no protection to young children in Western Kenya. PLoS One 4 3 (2009) e4708
57. Guevara Patino J.A., Holder A.A., McBride J.S., and Blackman M.J. Antibodies that inhibit malaria merozoite surface protein-1 processing and erythrocyte invasion are blocked by naturally acquired human antibodies. J Exp Med 186 November (10) (1997) 1689-1699
58. Holder A.A. The carboxy-terminus of merozoite surface protein 1: structure, specific antibodies and immunity to malaria. Parasitology 136 October (12) (2009) 1445-1456
59. Reed Z.H., Kieny M.P., Engers H., Friede M., Chang S., Longacre S., et al. Comparison of immunogenicity of five MSP1-based malaria vaccine candidate antigens in rabbits. Vaccine 27 March (10) (2009) 1651-1660
60. Bates J.T., Uematsu S., Akira S., and Mizel S.B. Direct stimulation of tlr5+/+ CD11c+ cells is necessary for the adjuvant activity of flagellin. J Immunol 182 June (12) (2009) 7539-7547
61. Means T.K., Hayashi F., Smith K.D., Aderem A., and Luster A.D. The toll-like receptor 5 stimulus bacterial flagellin induces maturation and chemokine production in human dendritic cells. J Immunol 170 May (10) (2003) 5165-5175
62. Sanders C.J., Franchi L., Yarovinsky F., Uematsu S., Akira S., Nunez G., et al. Induction of adaptive immunity by flagellin does not require robust activation of innate immunity. Eur J Immunol 39 February (2) (2009) 359-371
63. Vicente-Suarez I., Takahashi Y., Cheng F., Horna P., Wang H.W., Wang H.G., et al. Identification of a novel negative role of flagellin in regulating IL-10 production. Eur J Immunol 37 November (11) (2007) 3164-3175