Structural characterisation of sporozoite components for a multistage, multi-epitope, anti-malarial vaccine

International Journal of Biochemistry and Cell Biology

Volumn 40, Issue 3, 2008, Pages 543-557

  Patarroyo, Manuel E ^a,b   Cifuentes, Gladys ^a   Rodríguez, Raúl ^a  

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

^b UNIVERSIDAD NACIONAL DE COLOMBIA   (Colombia)

Author keywords

HLA DR 1* molecule; Malaria; MHC II peptide TCR complex; TRAP

Indexed keywords

EPITOPE; HIGH ACTIVITY BINDING PEPTIDE; HLA DR ANTIGEN; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; MALARIA VACCINE; SYNTHETIC PEPTIDE; T LYMPHOCYTE RECEPTOR; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANTIGEN BINDING; ARTICLE; BINDING AFFINITY; CONTROLLED STUDY; EXPERIMENTAL MODEL; IMMUNOGENICITY; INFECTION SENSITIVITY; LIVER CELL; MALARIA; MONKEY; NONHUMAN; PEPTIDE ANALYSIS; PROTEIN STRUCTURE; SPOROZOITE; STRUCTURE ANALYSIS; THREE DIMENSIONAL IMAGING;

ANIMALS; AOTIDAE; CRYSTALLOGRAPHY, X-RAY; EPITOPES; HLA-DR ANTIGENS; MALARIA VACCINES; MALARIA, FALCIPARUM; PEPTIDES; PLASMODIUM FALCIPARUM; PROTEIN CONFORMATION; PROTOZOAN PROTEINS; SPOROZOITES;

EID: 39049101482     PISSN: 13572725     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.biocel.2007.09.005     Document Type: Article

References (70)

1. Adams J.C., and Lawler J. The thrombospondins. Int. J. Biochem. Cell Biol. 36 (2004) 961-968
2. Adams J.C., and Tucker R.P. The thrombospondin type 1 repeat (TSR) superfamily: Diverse proteins with related roles in neuronal development. Dev. Dyn. 218 (2000) 280-299
3. Akhouri R.R., Bhattacharyya A., Pattnaik P., Malhotra P., and Sharma A. Structural and functional dissection of the adhesive domains of Plasmodium falciparum thrombospondin-related anonymous protein (TRAP). Biochem. J. 79 (2004) 815-822
4. Armen R., Alonso D.O., and Daggett V. The role of alpha-, 3(10)-, and pi-helix in helix--coil transitions. Protein Sci. 12 (2003) 1145-1157
5. Bax A., and Davis D.G. MLEV-17 based two dimensional homonuclear magnetisacion transfer spectroscopy. J. Magn. Reson. 65 (1985) 355-360
6. Bejon P., Mwacharo J., Kai O., Mwangi T., Milligan P., et al. A phase 2b randomised trial of the candidate malaria vaccines FP9 ME-TRAP and MVA ME-TRAP among children in Kenya. PLoS Clin. Trials 1 (2006) e29
7. Bozdech Z., Llinas M., Pulliam B.L., Wong D.L., Zhu J., and DeRisi J.L. The transcriptome of the intraerythrocytic developmental cycle of Plasmodium falciparum. PLoS Biol. 1 (2003) 1-16
8. Buscaglia C.A., Coppens I., Hol W.G., and Nussenzweig V. Sites of interaction between aldolase and thrombospondin-related anonymous protein in plasmodium. Mol. Biol. Cell. 14 (2003) 4947-4957
9. Charoenvit Y., Fallarme V., Rogers W.O., Sacci Jr. J.B., Kaur M., et al. Development of two monoclonal antibodies against Plasmodium falciparum sporozoite surface protein 2 and mapping of B-cell epitopes. Infect. Immun. 65 (1997) 3430-3437
10. Cifuentes G., Guzman F., Alba M.P., Salazar L.M., and Patarroyo M.E. Analysis of a Plasmodium falciparum EBA-175 peptide with high binding capacity to erythrocytes and their analogues using 1H NMR. J. Struct. Biol. 141 (2003) 115-121
11. Cifuentes G., Patarroyo M.E., Urquiza M., Ramírez L.E., Reyes C., and Rodríguez R. Distorting malaria peptide backbone structure to enable fitting into MHC class II molecules renders modified peptides immunogenic and protective. J. Med. Chem. 46 (2003) 2250-2253
12. Cigel F., Batchelder J., Burns Jr. J.M., Yanez D., van der Heyde H., et al. Immunity to blood-stage murine malarial parasites is MHC class II dependent. Immunol. Lett. 89 (2003) 243-249
13. Collins W.E., Warren M., Skinner J.C., Chin W., and Richardson B.B. Studies on the Santa Lucia (El Salvador) strain of Plasmodium falciparum in Aotus trivirgatus monkeys. J. Parasitol. 63 (1977) 52-56
14. Cubillos M., Espejo F., Purmova J., Martínez J.D., and Patarroyo M.E. Alpha helix shortening in 1522 MSP-1 conserved peptide analogs is associated with immunogenicity and protection against P. falciparum malaria. Proteins 50 (2003) 400-409
15. Emsley J., Cruz M., Handin R., and Liddington R. Crystal structure of the von Willebrand Factor A1 domain and implications for the binding of platelet glycoprotein Ib. J. Biol. Chem. 273 (1998) 10396-10401
16. Enea V., Ellis J., Zavala F., Arnot D.E., Asavanich A., et al. DNA cloning of Plasmodium falciparum circumsporozoite gene: Amino acid sequence of repetitive epitope. Science 225 (1984) 628-630
17. Espejo F., Cubillos M., Salazar L.M., Guzmán F., Urquiza M., et al. Structure, immunogenicity, and protectivity relationship for the 1585 malarial peptide and its substitution analogues. Angew. Chem. Int. Ed. Engl. 40 (2001) 4654-4657
18. Fidock D.A., Sallenave-Sales S., Sherwood J.A., Gachihi G.S., Ferreira-da-Cruz M.F., et al. Conservation of the Plasmodium falciparum sporozoite surface protein gene, STARP, in field isolates and distinct species of Plasmodium. Mol. Biochem. Parasitol. 67 (1994) 255-267
19. Fine E., Aikawa M., Cochrane A.H., and Nussenzweig R.S. Immuno-electron microscopic observations on Plasmodium knowlesi sporozoites: Localization of protective antigen and its precursors. Am. J. Trop. Med. Hyg. 33 (1984) 220-226
20. Frevert U. Sneaking in through the back entrance: The biology of malaria liver stages. Trends Parasitol. 20 (2004) 417-424
21. Gandon S., Mackinnon M.J., Nee S., and Read A.F. Imperfect vaccines and the evolution of pathogen virulence. Nature 414 (2001) 751-756
22. Garcia J.E., Puentes A., and Patarroyo M.E. Developmental biology of sporozoite-host interactions in Plasmodium falciparum malaria: Implications for vaccine design. Clin. Microbiol. Rev. 19 (2006) 686-707
23. Good M.F., Xu H., Wykes M., and Enqwerda C.R. Development and regulation of cell-mediated immune responses to the blood stages of malaria: Implications for vaccine research. Annu. Rev. Immunol. 23 (2005) 69-99
24. Good M.F., Zevering Y., Currier J., and Bilsborough J. 'Original antigenic sin', T cell memory, and malaria sporozoite immunity: An hypothesis for immune evasion. Parasite Immunol. 15 (1993) 187-193
25. Gruner A.C., Brahimi K., Eling W., Konings R., Meis J., et al. The Plasmodium falciparum knob-associated PfEMP3 antigen is also expressed at pre-erythrocytic stages and induces antibodies which inhibit sporozoite invasion. Mol. Biochem. Parasitol. 112 (2001) 253-261
26. Hernández E.C., Suárez C.F., Méndez J.A., Echeverry S.J., Murillo L.A., et al. Identification, cloning, and sequencing of different cytokine genes in four species of owl monkey. Immunogenetics 54 (2002) 645-653
27. Houghten R.A. General method for the rapid solid phase synthesis of large numbers of peptides: Specificity of antigen antibody interaction at the level of individual amino acids. Proc. Natl. Acad. Sci. U.S.A. 82 (1985) 5131-5135
28. Ishino T., Yano K., Chinzei Y., and Yuda M. Cell-passage activity is required for the malarial parasite to cross the liver sinusoidal cell layer. PLoS Biol. 2 (2004) 77-84
29. Jeener J., Meier B.H., Bachmann P., and Ernst R.R. Investigation of enhance processes by two dimensional NMR spectroscopy. J. Chem. Phys. 69 (1979) 4546-4553
30. Jewett T.J., and Sibley L.D. Aldolase forms a bridge between cell surface adhesins and the actin cytoskeleton in apicomplexan parasites. Mol. Cell. 11 (2003) 885-894
31. Kappe S., Bruderer S., Gantt S., Fujioka H., Nussenzweig V., and Menard R. Conservation of a gliding motility and cell invasion machinery in Apicomplexan parasites. J. Cell. Biol. 147 (1999) 937-944
32. Kappe S.H., Buscaglia C.A., and Nussenzweig V. Plasmodium sporozoite molecular cell biology. Annu. Rev. Cell. Dev. Biol. 20 (2004) 29-59
33. López R., Curtidor H., Urquiza M., García J., Puentes A., et al. Plasmodium falciparum: Binding studies of peptide derived from the sporozoite surface protein 2 to Hep G2 cells 58 (2001) 285-292
34. Marsh S.G., Parham P., and Barber L.D. The HLA Facts Book (2000), Academic Press, New York
35. Matuschewski K., Nunes A.C., Nussenzweig V., and Menard R. Plasmodium sporozoite invasion into insect and mammalian cells is directed by the same dual binding system. EMBO J. 21 (2002) 1597-1606
36. McCormick C.J., Tuckwell D.S., Crisanti A., Humphries M.J., et al. Identification of heparin as a ligand for the A-domain of Plasmodium falciparum thrombospondin-related adhesion protein. Mol. Biochem. Parasitol. 100 (1999) 111-124
37. Merrifield B. Concept and early development of solid-phase peptide synthesis. Methods Enzymol. 289 (1997) 3-13
38. Moncada C.A., Guerrero E., Cardenas P., Suárez C.F., Patarroyo M.E., et al. The T-cell receptor in primates: Identifying and sequencing new owl monkey TRBV gene sub-groups. Immunogenetics 57 (2005) 42-52
39. Mota M.M., Giordano S., and Rodriguez A. Targeting Plasmodium host cells: Survival within hepatocytes. Trends Mol. Med. 10 (2004) 487-492
40. Mota M.M., Hafalla J.C., and Rodriguez A. Migration through host cells activates Plasmodium sporozoites for infection. Nat. Med. 8 (2002) 1318-1322
41. Mota M.M., Pradel G., Vanderberg J.P., Hafalla J.C., Frevert U., et al. Migration of Plasmodium sporozoites through cells before infection. Science 291 (2001) 24-25
42. Muller H.M., Reckmann I., Hollingdale M.R., Bujard H., Robson K.J., and Crisanti A. Thrombospondin related anonymous protein (TRAP) of Plasmodium falciparum binds specifically to sulfated glycoconjugates and to HepG2 hepatoma cells suggesting a role for this molecule in sporozoite invasion of hepatocytes. EMBO J. 12 (1993) 2881-2889
43. Nardin E.H., Oliveira G.A., Calvo-Calle J.M., and Nussenzweig R.S. The use of multiple antigen peptides in the analysis and induction of protective immune responses against infectious diseases. Adv. Immunol. 60 (1995) 105-149
44. Paakkonen K., Tossavainen H., Permi P., Rakkolainen H., Rauvala H., et al. Solution structures of the first and fourth TSR domains of F-spondin. Proteins 64 (2006) 665-672
45. Patarroyo M.E., Alba M.P., Vargas L.E., Silva Y., Rosas J., et al. Peptides inducing short-lived antibody responses against Plasmodium falciparum malaria have shorter structures and are read in a different MHC II functional register. Biochemistry 44 (2005) 6745-6754
46. Patarroyo M.E., Cifuentes G., and Baquero J. Comparative molecular and three-dimensional analysis of the peptide-MHC II binding region in both human and Aotus MHC-DRB molecules confirms their usefulness in antimalarial vaccine development. Immunogenetics 58 (2006) 598-606
47. Patarroyo M.E., Cifuentes G., Vargas L.E., and Rosas J. Structural modifications enable conserved peptides to fit into MHC molecules thus inducing protection against malaria. Chembiochem 5 (2004) 1588-1593
48. Pico de Coaña Y., Guerrero E., Barrero C., Rodríguez J., Rodríguez R., et al. A highly infective Plasmodium vivax strain adapted to Aotus monkeys: Quantitative haematological and molecular determinations useful for P. vivax malaria vaccine development. Vaccine 21 (2003) 3930-3937
49. Pradel G., Garapaty S., and Frevert U. Proteoglycans mediate malaria sporozoite targeting to the liver. Mol. Microbiol. 45 (2002) 637-651
50. Rammensee H.G., Friede T., and Stevanoviic S. MHC ligands and peptide motifs: First listing. Immunogenetics 41 (1995) 178-228
51. Rance M., Sorensen O.W., Bodenhausen G., Wagner G., Ernst R.R., and Wüthrich K. Improved spectral resolution in cosy 1H NMR spectra of proteins via double quantum filtering. Biochem. Biophys. Res. Commun. 117 (1983) 479-485
52. Robson K.J., Frebert U., Reckmann I., Cowan G., Beier J., et al. Thrombospondin-related adhesive protein (TRAP) of Plasmodium falciparum: Expression during sporozoite ontogeny and binding to human hepatocytes. EMBO J. 14 (1995) 3883-3894
53. Robson K.J., Hall J.R., Davies L.C., Crisanti A., Hill A.V., and Wellems T.E. Polymorphism of the TRAP gene of Plasmodium falciparum. Proc. R. Soc. Lond. B 242 (1990) 205-216
54. Robson K.J., Hall J.R., Jennings M.W., Harris T.J., Marsh K., et al. A highly conserved amino-acid sequence in thrombospondin, properdin and in proteins from sporozoites and blood stages of a human malaria parasite. Nature 335 (1988) 79-82
55. Rodriguez R., Moreno A., Guzman F., Calvo M., and Patarroyo M.E. Studies in owl monkeys leading to the development of a synthetic vaccine against the asexual blood stages of Plasmodium falciparum. Am. J. Trop. Med. Hyg. 43 (1990) 339-354
56. Rogers W.O., Malik A., Mellouk S., Nakamura K., Rogers M.D., et al. Characterization of Plasmodium falciparum sporozoite surface protein 2. Proc. Natl. Acad. Sci. U.S.A. 89 (1992) 9176-9180
57. Rohl C.A., and Doig A.J. Models for the 3(10)-helix/coil, pi-helix/coil, and alpha-helix/3(10)-helix/coil transitions in isolated peptides. Protein Sci. 5 (1996) 1687-1696
58. Sinigaglia F., Romagnoli P., Guttinger M., Takacs B., and Pink J.R. Selection of T-cell epitopes and vaccine engineering. Methods Enzymol. 203 (1991) 370-386
59. Snow R.W., Guerra C.A., Noor A.M., Myint H.Y., and Hay S.I. The global distribution of clinical episodes of Plasmodium falciparum malaria. Nature 434 (2005) 214-217
60. Starnes G.L., Jewett T.J., Carruthers V.B., and Sibley L.D. Two separate, conserved acidic amino acid domains within the Toxoplasma gondii MIC2 cytoplasmic tail are required for parasite survival. J. Biol. Chem. 281 (2006) 30745-30754
61. Suárez C.F., Patarroyo M.E., Trujillo E., Estupiñán M., Baquero J.E., et al. Owl monkey MHC-DRB exon 2 reveals high similarity with several HLA-DRB lineages. Immunogenetics 58 (2006) 542-558
62. Sultan A.A., Thathy V., Frevert U., Robson K.J., Crisanti A., et al. TRAP is necessary for gliding motility and infectivity of plasmodium sporozoites. Cell 90 (1997) 511-522
63. Tan K., Duquette M., Liu J.H., Dong Y., Zhang R., et al. Crystal structure of the TSP-1 type 1 repeats: A novel layered fold and its biological implication. J. Cell. Biol. 159 (2002) 373-382
64. Tossavainen H., Pihlajamaa T., Huttunen T.K., Raulo E., Rauvala H., et al. The layered fold of the TSR domain of P. falciparum TRAP contains a heparin binding site. Protein Sci. 15 (2006) 1760-1768
65. Trottein F., Triglia T., and Cowman A.F. Molecular cloning of a gene from Plasmodium falciparum that codes for a protein sharing motifs found in adhesive molecules from mammals and plasmodia. Mol. Biochem. Parasitol. 74 (1995) 129-141
66. Tucker R.P. The thrombospondin type 1 repeat superfamily. Int. J. Biochem. Cell. Biol. 36 (2004) 969-974
67. Vargas L.E., Parra C.A., Salazar L.M., Guzman F., Pinto M., et al. MHC allele specific binding of a malaria peptide makes it become promiscuous on fitting a glycine residue into Pocket-6. Biochem. Biophys Res. Commun. 307 (2003) 48-56
68. Wengelnik K., Spaccapelo R., Naitza S., Robson K.J., Janse C.J., et al. The A-domain and the thrombospondin-related motif of Plasmodium falciparum TRAP are implicated in the invasion process of mosquito salivary glands. EMBO J. 18 (1999) 5195-5204
69. Whittaker C.A., and Hynes R.O. Distribution and evolution of von Willebrand/integrin A domains: Widely dispersed domains with roles in cell adhesion and elsewhere. Mol. Biol. Cell. 13 (2002) 3369-3387
70. Yuda M., and Ishino T. Liver invasion by malarial parasites-how do malarial parasites break through the host barrier?. Cell Microbiol. 6 (2004) 1119-1125