Hostname: page-component-8448b6f56d-c47g7 Total loading time: 0 Render date: 2024-04-23T22:32:04.260Z Has data issue: false hasContentIssue false
  • English
  • Français

Selection of peptides recognized by human antibodies against the surface of Plasmodium falciparum-infected erythrocytes

Published online by Cambridge University Press:  13 December 2004

S. EDA  and
I. W. SHERMAN
S. EDA
Affiliation:
Department of Biology, University of California Riverside, Riverside, California 92521, USA Present address: Department of Forestry, Wildlife and Fisheries, University of Tennessee Knoxville, Knoxville, Tennessee 37996, USA.
I. W. SHERMAN
Affiliation:
Department of Biology, University of California Riverside, Riverside, California 92521, USA
Get access Rights & Permissions [Opens in a new window]

Abstract

In an attempt to identify mimotopes of the surface antigens of P. falciparum-infected erythrocytes (iRBC), antibodies were eluted from iRBC that had been treated with a pool of sera from malaria-infected individuals (IHS), and were used to screen a phage display library (PDL). After repeated panning of the PDL on immobilized antibodies, phage that selectively bound to IHS were accumulated. Of 23 randomly chosen clones that were sequenced, 13 individual sequences were detected at varying frequencies and 3 of the 13 sequences had homology with membrane proteins known to exist on iRBC. The majority of phage clones (7 out of 8 clones) selected after the 4th panning bound selectively to IgG in IHS. Specific binding of the selected phage to IgG in IHS was also confirmed using 24 IHS and 11 sera from uninfected individuals. One phage clone was the most frequently found in the sequenced clones after the 4th panning, and the binding of this clone to IgG in all IHS was greater than in any serum from uninfected individuals. A rabbit antiserum against the peptide expressed on the clone specifically recognized the surface of iRBC and resulted in iRBC haemolysis.

Keywords

Plasmodium falciparumerythrocytesurface antigenphage display library
Type
Research Article
Information
Parasitology , Volume 130 , Issue 1 , January 2005 , pp. 1 - 11
Copyright
© 2004 Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

AIKAWA, M., RABBEGE, J. R., UDEINYA, I. & MILLER, L. H. ( 1983). Electron microscopy of knobs in Plasmodium falciparum-infected erythrocytes. Journal of Parasitology 69, 435–437.CrossRefGoogle Scholar
ARAP, W., KOLONIN, M. G., TREPEL, M., LAHDENRANTA, J., CARDO-VILA, M., GIORDANO, R. J., MINTZ, P. J., ARDELT, P. U., YAO, V. J., VIDAL, C. I., CHEN, L., FLAMM, A., VALTANEN, H., WEAVIND, L. M., HICKS, M. E., POLLOCK, R. E., BOTZ, G. H., BUCANA, C. D., KOIVUNEN, E., CAHILL, D., TRONCOSO, P., BAGGERLY, K. A., PENTZ, R. D., DO, K. A., LOGOTHETIS, C. J. & PASQUALINI, R. ( 2002). Steps toward mapping the human vasculature by phage display. Nature Medicine 8, 121–127.CrossRefGoogle Scholar
BAIRD, J. K. ( 1998). Age-dependent characteristics of protection v. susceptibility to Plasmodium falciparum. Annals of Tropical Medicine and Parasitology 92, 367–390.CrossRefGoogle Scholar
BARUCH, D. I., PASLOSKE, B. L., SINGH, H. B., BI, X., MA, X. C., FELDMAN, M., TARASCHI, T. F. & HOWARD, R. J. ( 1995). Cloning the P. falciparum gene encoding PfEMP1, a malarial variant antigen and adherence receptor on the surface of parasitized human erythrocytes. Cell 82, 77–87.Google Scholar
BARUCH, D. I., GAMAIN, B., BARNWELL, J. W., SULLIVAN, J. S., STOWERS, A., GALLAND, G. G., MILLER, L. H. & COLLINS, W. E. ( 2002 a). Immunization of Aotus monkeys with a functional domain of the Plasmodium falciparum variant antigen induces protection against a lethal parasite line. Proceedings of the National Academy of Sciences, USA 99, 3860–3865.Google Scholar
BARUCH, D. I., ROGERSON, S. J. & COOKE, B. M. ( 2002 b). Asexual blood stages of malaria antigens: cytoadherence. Chemical Immunology 80, 144–162.Google Scholar
BEESON, J. G. & BROWN, G. V. ( 2002). Pathogenesis of Plasmodium falciparum malaria: the roles of parasite adhesion and antigenic variation. Cellular and Molecular Life Sciences 59, 258–271.CrossRefGoogle Scholar
BOWDITCH, R. D., TANI, P., FONG, K. C. & McMILLAN, R. ( 1996). Characterization of autoantigenic epitopes on platelet glycoprotein IIb/IIIa using random peptide libraries. Blood 88, 4579–4584.Google Scholar
CLYDE, D. F., MOST, H., McCARTHY, V. C. & VANDERBERG, J. P. ( 1973). Immunization of man against sporozite-induced falciparum malaria. American Journal of the Medical Sciences 266, 169–177.CrossRefGoogle Scholar
COCHRANE, A. H., AIKAWA, M., JENG, M. & NUSSENZWEIG, R. S. ( 1976). Antibody-induced ultrastructural changes of malarial sporozoites. Journal of Immunology 116, 859–867.Google Scholar
CRANDALL, I., GUTHRIE, N. & SHERMAN, I. W. ( 1995). Plasmodium falciparum: sera of individuals living in a malaria-endemic region recognize peptide motifs of the human erythrocyte anion transport protein. American Journal of Tropical Medicine and Hygiene 52, 450–455.CrossRefGoogle Scholar
DA SILVA, A. Jr., KAWAZOE, U., FREITAS, F. F., GATTI, M. S., DOLDER, H., SCHUMACHER, R. I., JULIANO, M. A., DA SILVA, M. J. & LEITE, A. ( 2002). Avian anticoccidial activity of a novel membrane-interactive peptide selected from phage display libraries. Molecular and Biochemical Parasitology 120, 53–60.CrossRefGoogle Scholar
DEMANGEL, C., ROUYRE, S., ALZARI, P. M., NATO, F., LONGACRE, S., LAFAYE, P. & MAZIE, J. C. ( 1998). Phage-displayed mimotopes elicit monoclonal antibodies specific for a malaria vaccine candidate. Biological Chemistry 379, 65–70.Google Scholar
DOOLAN, D. L. & HOFFMAN, S. L. ( 2002). Nucleic acid vaccines against malaria. Chemical Immunology 80, 308–321.CrossRefGoogle Scholar
EDA, S., EDA, K., PRUDHOMME, J. G. & SHERMAN, I. W. ( 1999). Inhibitory activity of human lactoferrin and its peptide on chondroitin sulfate A-, CD36-, and thrombospondin-mediated cytoadherence of Plasmodium falciparum-infected erythrocytes. Blood 94, 326–332.Google Scholar
EDA, S. & SHERMAN, I. W. ( 2002). Cytoadherence of malaria-infected red blood cells involves exposure of phosphatidylserine. Cellular Physiology and Biochemistry 12, 373–384.CrossRefGoogle Scholar
FREITAS-JUNIOR, L. H., BOTTIUS, E., PIRRIT, L. A., DEITSCH, K. W., SCHEIDIG, C., GUINET, F., NEHRBASS, U., WELLEMS, T. E. & SCHERF, A. ( 2000). Frequent ectopic recombination of virulence factor genes in telomeric chromosome clusters of P. falciparum. Nature, London 407, 1018–1022.Google Scholar
GAMAIN, B., MILLER, L. H. & BARUCH, D. I. ( 2001). The surface variant antigens of Plasmodium falciparum contain cross-reactive epitopes. Proceedings of the National Academy of Sciences, USA 98, 2664–2669.CrossRefGoogle Scholar
GARDNER, M. J., HALL, N., FUNG, E., WHITE, O., BERRIMAN, M., HYMAN, R. W., CARLTON, J. M., PAIN, A., NELSON, K. E., BOWMAN, S., PAULSEN, I. T., JAMES, K., EISEN, J. A., RUTHERFORD, K., SALZBERG, S. L., CRAIG, A., KYES, S., CHAN, M. S., NENE, V., SHALLOM, S. J., SUH, B., PETERSON, J., ANGIUOLI, S., PERTEA, M., ALLEN, J., SELENGUT, J., HAFT, D., MATHER, M. W., VAIDYA, A. B., MARTIN, D. M., FAIRLAMB, A. H., FRAUNHOLZ, M. J., ROOS, D. S., RALPH, S. A., McFADDEN, G. I., CUMMINGS, L. M., SUBRAMANIAN, G. M., MUNGALL, C., VENTER, J. C., CARUCCI, D. J., HOFFMAN, S. L., NEWBOLD, C., DAVIS, R. W., FRASER, C. M. & BARRELL, B. ( 2002). Genome sequence of the human malaria parasite Plasmodium falciparum. Nature, London 419, 498–511.CrossRefGoogle Scholar
HEDDINI, A. ( 2002). Malaria pathogenesis: a jigsaw with an increasing number of pieces. International Journal for Parasitology 32, 1587–1598.CrossRefGoogle Scholar
KAY, M. M. ( 1992). Molecular mapping of human band 3 aging antigenic sites and active amino acids using synthetic peptides. Journal of Protein Chemistry 11, 595–602.CrossRefGoogle Scholar
KOIVUNEN, E., GAY, D. A. & RUOSLAHTI, E. ( 1993). Selection of peptides binding to the alpha 5 beta 1 integrin from phage display library. Journal of Biological Chemistry 268, 20205–20210.Google Scholar
KUMAR, S., EPSTEIN, J. E. & RICHIE, T. L. ( 2002). Vaccines against asexual stage malaria parasites. Chemical Immunology 80, 262–286.CrossRefGoogle Scholar
LAMBROS, C. & VANDERBERG, J. P. ( 1979). Synchronization of Plasmodium falciparum erythrocytic stages in culture. Journal of Parasitology 65, 418–420.CrossRefGoogle Scholar
MAGUIRE, P. A. & SHERMAN, I. W. ( 1990). Phospholipid composition, cholesterol content and cholesterol exchange in Plasmodium falciparum-infected red cells. Molecular and Biochemical Parasitology 38, 105–112.CrossRefGoogle Scholar
MAGUIRE, P. A., PRUDHOMME, J. & SHERMAN, I. W. ( 1991). Alterations in erythrocyte membrane phospholipid organization due to the intracellular growth of the human malaria parasite, Plasmodium falciparum. Parasitology 102, 179–186.CrossRefGoogle Scholar
MOORE, S. A., SURGEY, E. G. & CADWGAN, A. M. ( 2002). Malaria vaccines: where are we and where are we going? Lancet Infectious Diseases 2, 737–743.Google Scholar
NAGAO, E., KANEKO, O. & DVORAK, J. A. ( 2000). Plasmodium falciparum-infected erythrocytes: qualitative and quantitative analyses of parasite-induced knobs by atomic force microscopy. Journal of Structural Biology 130, 34–44.CrossRefGoogle Scholar
PASVOL, G., WILSON, R. J., SMALLEY, M. E. & BROWN, J. ( 1978). Separation of viable schizont-infected red cells of Plasmodium falciparum from human blood. Annals of Tropical Medicine and Parasitology 72, 87–88.CrossRefGoogle Scholar
RENKONEN, R., FUKUDA, M. N., PETROV, L., PAAVONEN, T., RENKONEN, J., HAYRY, P. & FUKUDA, M. ( 2002). A peptide mimic of selectin ligands abolishes in vivo inflammation but has no effect on the rat heart allograft survival. Transplantation 74, 2–6.CrossRefGoogle Scholar
RHEE, M. S., AKANMORI, B. D., WATERFALL, M. & RILEY, E. M. ( 2001). Changes in cytokine production associated with acquired immunity to Plasmodium falciparum malaria. Clinical and Experimental Immunology 126, 503–510.CrossRefGoogle Scholar
SABCHAREON, A., BURNOUF, T., OUATTARA, D., ATTANATH, P., BOUHAROUN-TAYOUN, H., CHANTAVANICH, P., FOUCAULT, C., CHONGSUPHAJAISIDDHI, T. & DRUILHE, P. ( 1991). Parasitologic and clinical human response to immunoglobulin administration in falciparum malaria. American Journal of Tropical Medicine and Hygiene 45, 297–308.CrossRefGoogle Scholar
SAMOYLOVA, T. I., AHMED, B. Y., VODYANOY, V., MORRISON, N. E., SAMOYLOV, A. M., GLOBA, L. P., BAKER, H. J. & COX, N. R. ( 2002). Targeting peptides for microglia identified via phage display. Journal of Neuroimmunology 127, 13–21.CrossRefGoogle Scholar
SANTAMARIA, H., MANOUTCHARIAN, K., ROCHA, L., GONZALEZ, E., ACERO, G., GOVEZENSKY, T., URIBE, L. I., OLGUIN, A., PANIAGUA, J. & GEVORKIAN, G. ( 2001). Identification of peptide sequences specific for serum antibodies from human papillomavirus-infected patients using phage display libraries. Clinical Immunology 101, 296–302.CrossRefGoogle Scholar
SCOTT, J. K. & SMITH, G. P. ( 1990). Searching for peptide ligands with an epitope library. Science 249, 386–390.CrossRefGoogle Scholar
SHERMAN, I. W., CRANDALL, I. & SMITH, H. ( 1992). Membrane proteins involved in the adherence of Plasmodium falciparum-infected erythrocytes to the endothelium. Biology of the Cell 74, 161–178.CrossRefGoogle Scholar
SHERMAN, I. W., EDA, S. & WINOGRAD, E. ( 2003). Cytoadherence and sequestration in Plasmodium falciparum: defining the ties that bind. Microbes and Infection 5, 897–909.CrossRefGoogle Scholar
SMITH, J. D., GAMAIN, B., BARUCH, D. I. & KYES, S. ( 2001). Decoding the language of var genes and Plasmodium falciparum sequestration. Trends in Parasitology 17, 538–545.CrossRefGoogle Scholar
TRAGER, W. & JENSEN, J. B. ( 1976). Human malaria parasites in continuous culture. Science 193, 673–675.CrossRefGoogle Scholar
TRIGG, P. & KONDRACHINE, A. ( 1998). The current global malaria situation. In Malaria: Parasite Biology, Pathogenesis and Protection ( ed. Sherman, I. W.), pp. 11–22. ASM Press, Washington, D.C.
WILLIS, A. E., PERHAM, R. N. & WRAITH, D. ( 1993). Immunological properties of foreign peptides in multiple display on a filamentous bacteriophage. Gene 128, 79–83.CrossRefGoogle Scholar
WINOGRAD, E., EDA, S. & SHERMAN, I. W. ( 2004). Chemical modifications of band 3 protein affect the adhesion of Plasmodium falciparum-infected erythrocytes to CD36. Molecular and Biochemical Parasitology 136, 243–248.CrossRefGoogle Scholar
ZHU, Q., LEE, D. W. & CASEY, J. R. ( 2003). Novel topology in C-terminal region of the human plasma membrane anion exchanger, AE1. Journal of Biological Chemistry 278, 3112–3120.CrossRefGoogle Scholar