Hostname: page-component-cd9895bd7-jn8rn Total loading time: 0 Render date: 2024-12-23T13:58:37.205Z Has data issue: false hasContentIssue false
  • English
  • Français

The carboxy-terminus of merozoite surface protein 1: structure, specific antibodies and immunity to malaria

Published online by Cambridge University Press:  23 July 2009

A. A. HOLDER
A. A. HOLDER*
Affiliation:
Division of Parasitology, MRC National Institute for Medical Research, The Ridgeway, Mill Hill, London NW7 1AA
*
*Tel: +44 208 8162175. Fax: +44 208 8162730. E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Summary

Over the last 30 years, evidence has been gathered suggesting that merozoite surface protein 1 (MSP1) is a target of protective immunity against malaria. In a variety of experimental approaches using in vitro methodology, animal models and sero-epidemiological techniques, the importance of antibody against MSP1 has been established but we are still finding out what are the mechanisms involved. Now that clinical trials of MSP1 vaccines are underway and the early results have been disappointing, it is increasingly clear that we need to know more about the mechanisms of immunity, because a better understanding will highlight the limitations of our current assays and identify the improvements required. Understanding the structure of MSP1 will help us design and engineer better antigens that are more effective than the first generation of vaccine candidates. This review is focused on the carboxy-terminus of MSP1.

Keywords

malariamerozoiteMSP1structureantibody
Type
Research Article
Information
Parasitology , Volume 136 , Special Issue 12: Special Centenary Issue – Parasitology 1908–2008 , October 2009 , pp. 1445 - 1456
Copyright
Copyright © Cambridge University Press 2009

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

Arnot, D. E., Cavanagh, D. R., Remarque, E. J., Creasey, A. M., Sowa, M. P., Morgan, W. D., Holder, A. A., Longacre, S. and Thomas, A. W. (2008). Comparative testing of six antigen-based malaria vaccine candidates directed toward merozoite-stage Plasmodium falciparum. Clinical and Vaccine Immunology 15, 1345–1355.CrossRefGoogle ScholarPubMed
Babon, J. J., Morgan, W. D., Kelly, G., Eccleston, J. F., Feeney, J. and Holder, A. A. (2007). Structural studies on Plasmodium vivax merozoite surface protein-1. Molecular and Biochemical Parasitology 153, 31–40.CrossRefGoogle ScholarPubMed
Barale, J. C., Blisnick, T., Fujioka, H., Alzari, P. M., Aikawa, M., Braun-Breton, C. and Langsley, G. (1999). Plasmodium falciparum subtilisin-like protease 2, a merozoite candidate for the merozoite surface protein 1-42 maturase. Proceedings of the National Academy of Sciences, USA 96, 6445–6450.CrossRefGoogle ScholarPubMed
Benjamin, P. A., Ling, I. T., Clottey, G., Valero, L. M., Ogun, S. A., Fleck, S. L., Walliker, D., Morgan, W. D., Birdsall, B., Feeney, J. and Holder, A. A. (1999). Antigenic and sequence diversity at the C-terminus of the merozoite surface protein-1 from rodent malaria isolates, and the binding of protective monoclonal antibodies. Molecular and Biochemical Parasitology 104, 147–156.CrossRefGoogle ScholarPubMed
Bergmann-Leitner, E. S., Duncan, E. H., Mullen, G. E., Burge, J. R., Khan, F., Long, C. A., Angov, E. and Lyon, J. A. (2006). Critical evaluation of different methods for measuring the functional activity of antibodies against malaria blood stage antigens. American Journal of Tropical Medicine and Hygiene 75, 437–442.CrossRefGoogle ScholarPubMed
Blackman, M. J., Heidrich, H. G., Donachie, S., McBride, J. S. and Holder, A. A. (1990). 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. Journal of Experimental Medicine 172, 379–382.CrossRefGoogle ScholarPubMed
Blackman, M. J., Ling, I. T., Nicholls, S. C. and Holder, A. A. (1991). Proteolytic processing of the Plasmodium falciparum merozoite surface protein-1 produces a membrane-bound fragment containing two epidermal growth factor-like domains. Molecular and Biochemical Parasitology 49, 29–33.CrossRefGoogle ScholarPubMed
Blackman, M. J., Scott-Finnigan, T. J., Shai, S. and Holder, A. A. (1994). Antibodies inhibit the protease-mediated processing of a malaria merozoite surface protein. Journal of Experimental Medicine 180, 389–393.CrossRefGoogle ScholarPubMed
Burns, J. M. Jr., Daly, T. M., Vaidya, A. B. and Long, C. A. (1988). The 3' portion of the gene for a Plasmodium yoelii merozoite surface antigen encodes the epitope recognized by a protective monoclonal antibody. Proceedings of the Nationall Academy of Sciences, USA 85, 602–606.CrossRefGoogle ScholarPubMed
Chitarra, V., Holm, I., Bentley, G. A., Petres, S. and Longacre, S. (1999). The crystal structure of C-terminal merozoite surface protein 1 at 1·8 A resolution, a highly protective malaria vaccine candidate. Molecular Cell 3, 457–464.CrossRefGoogle ScholarPubMed
Corran, P. H., O'Donnell, R. A., Todd, J., Uthaipibull, C., Holder, A. A., Crabb, B. S. and Riley, E. M. (2004). The fine specificity, but not the invasion inhibitory activity, of 19-kilodalton merozoite surface protein 1-specific antibodies is associated with resistance to malarial parasitemia in a cross-sectional survey in The Gambia. Infection and Immunity 72, 6185–6189.CrossRefGoogle ScholarPubMed
Daly, T. M. and Long, C. A. (1993). A recombinant 15-kilodalton carboxyl-terminal fragment of Plasmodium yoelii yoelii 17XL merozoite surface protein 1 induces a protective immune response in mice. Infection and Immunity 61, 2462–2467.CrossRefGoogle ScholarPubMed
de Koning-Ward, T. F., O'Donnell, R. A., Drew, D. R., Thomson, R., Speed, T. P. and Crabb, B. S. (2003). A new rodent model to assess blood stage immunity to the Plasmodium falciparum antigen merozoite surface protein 119 reveals a protective role for invasion inhibitory antibodies. Journal of Experimental Medicine 198, 869–875.CrossRefGoogle Scholar
Dekker, C., Uthaipibull, C., Calder, L. J., Lock, M., Grainger, M., Morgan, W. D., Dodson, G. G. and Holder, A. A. (2004). Inhibitory and neutral antibodies to Plasmodium falciparum MSP119 form ring structures with their antigen. Molecular and Biochemical Parasitology 137, 143–149.CrossRefGoogle ScholarPubMed
Dluzewski, A. R., Ling, I. T., Hopkins, J. M., Grainger, M., Margos, G., Mitchell, G. H., Holder, A. A. and Bannister, L. H. (2008). Formation of the food vacuole in Plasmodium falciparum: a potential role for the 19 kDa fragment of merozoite surface protein 1 (MSP1(19)). PLoS ONE 3, e3085.CrossRefGoogle Scholar
Dodoo, D., Aikins, A., Kusi, K. A., Lamptey, H., Remarque, E., Milligan, P., Bosomprah, S., Chilengi, R., Osei, Y. D., Akanmori, B. D. and Theisen, M. (2008). Cohort study of the association of antibody levels to AMA1, MSP119, MSP3 and GLURP with protection from clinical malaria in Ghanaian children. Malaria Journal 7, 142.CrossRefGoogle ScholarPubMed
Dodoo, D., Theander, T. G., Kurtzhals, J. A., Koram, K., Riley, E., Akanmori, B. D., Nkrumah, F. K. and Hviid, L. (1999). Levels of antibody to conserved parts of Plasmodium falciparum merozoite surface protein 1 in Ghanaian children are not associated with protection from clinical malaria. Infection and Immunity 67, 2131–2137.CrossRefGoogle Scholar
Draper, S. J., Moore, A. C., Goodman, A. L., Long, C. A., Holder, A. A., Gilbert, S. C., Hill, F. and Hill, A. V. (2008). Effective induction of high-titer antibodies by viral vector vaccines. Nature Medicine 14, 819–821.CrossRefGoogle ScholarPubMed
Egan, A., Waterfall, M., Pinder, M., Holder, A. and Riley, E. (1997). Characterization of human T- and B-cell epitopes in the C terminus of Plasmodium falciparum merozoite surface protein 1: evidence for poor T- cell recognition of polypeptides with numerous disulfide bonds. Infection and Immunity 65, 3024–3031.CrossRefGoogle Scholar
Egan, A. F., Morris, J., Barnish, G., Allen, S., Greenwood, B. M., Kaslow, D. C., Holder, A. A. and Riley, E. M. (1996). Clinical immunity to Plasmodium falciparum malaria is associated with serum antibodies to the 19-kDa C-terminal fragment of the merozoite surface antigen, PfMSP-1. Journal of Infectious Diseases 173, 765–769.CrossRefGoogle Scholar
Faber, B. W., Remarque, E. J., Morgan, W. D., Kocken, C. H., Holder, A. A. and Thomas, A. W. (2007). Malaria vaccine-related benefits of a single protein comprising Plasmodium falciparum apical membrane antigen 1 domains I and II fused to a modified form of the 19-kilodalton C-terminal fragment of merozoite surface protein 1. Infection and Immunity 75, 5947–5955.CrossRefGoogle ScholarPubMed
Garman, S. C., Simcoke, W. N., Stowers, A. W. and Garboczi, D. N. (2003). Structure of the C-terminal domains of merozoite surface protein-1 from Plasmodium knowlesi reveals a novel histidine binding site. Journal of Biological Chemistry 278, 7264–7269.CrossRefGoogle ScholarPubMed
Gilson, P. R., O'Donnell, R. A., Nebl, T., Sanders, P. R., Wickham, M. E., McElwain, T. F., de Koning-Ward, T. F. and Crabb, B. S. (2008). MSP1(19) miniproteins can serve as targets for invasion inhibitory antibodies in Plasmodium falciparum provided they contain the correct domains for cell surface trafficking. Molecular Microbiology 68, 124–138.CrossRefGoogle ScholarPubMed
Goel, V. K., Li, X., Chen, H., Liu, S. C., Chishti, A. H. and Oh, S. S. (2003). Band 3 is a host receptor binding merozoite surface protein 1 during the Plasmodium falciparum invasion of erythrocytes. Proceedings of the National Academy of Sciences, USA 100, 5164–5169.CrossRefGoogle ScholarPubMed
Green, T. J., Morhardt, M., Brackett, R. G. and Jacobs, R. L. (1981). Serum inhibition of merozoite dispersal from Plasmodium falciparum schizonts: indicator of immune status. Infection and Immunity 31, 1203–1208.CrossRefGoogle ScholarPubMed
Guevara Patino, J. A., Holder, A. A., McBride, J. S. and Blackman, M. J. (1997). Antibodies that inhibit malaria merozoite surface protein-1 processing and erythrocyte invasion are blocked by naturally acquired human antibodies. Journal of Experimental Medicine 186, 1689–1699.CrossRefGoogle ScholarPubMed
Hackett, F., Sajid, M., Withers-Martinez, C., Grainger, M. and Blackman, M. J. (1999). PfSUB-2: a second subtilisin-like protein in Plasmodium falciparum merozoites. Molecular and Biochemical Parasitology 103, 183–195.CrossRefGoogle ScholarPubMed
Harris, P. K., Yeoh, S., Dluzewski, A. R., O'Donnell, R. A., Withers-Martinez, C., Hackett, F., Bannister, L. H., Mitchell, G. H. and Blackman, M. J. (2005). Molecular identification of a malaria merozoite surface sheddase. PLoS Pathogens 1, 241–251.CrossRefGoogle ScholarPubMed
Hensmann, M., Li, C., Moss, C., Lindo, V., Greer, F., Watts, C., Ogun, S. A., Holder, A. A. and Langhorne, J. (2004). Disulfide bonds in merozoite surface protein 1 of the malaria parasite impede efficient antigen processing and affect the in vivo antibody response. European Journal of Immunology 34, 639–648.CrossRefGoogle ScholarPubMed
Holder, A. A. and Freeman, R. R. (1981). Immunization against blood-stage rodent malaria using purified parasite antigens. Nature, London 294, 361–364.CrossRefGoogle ScholarPubMed
Holder, A. A. and Freeman, R. R. (1982). Biosynthesis and processing of a Plasmodium falciparum schizont antigen recognized by immune serum and a monoclonal antibody. Journal of Experimental Medicine 156, 1528–1538.CrossRefGoogle ScholarPubMed
Holder, A. A., Guevara Patino, J. A., Uthaipibull, C., Syed, S. E., Ling, I. T., Scott-Finnigan, T. and Blackman, M. J. (1999). Merozoite surface protein 1, immune evasion, and vaccines against asexual blood stage malaria. Parassitologia 41, 409–414.Google ScholarPubMed
Holder, A. A., Lockyer, M. J. and Hardy, G. W. (1988). A hybrid gene to express protein epitopes from both sporozoite and merozoite surface antigens of Plasmodium falciparum. Parasitology 97, 373–382.CrossRefGoogle ScholarPubMed
Holder, A. A., Lockyer, M. J., Odink, K. G., Sandhu, J. S., Riveros-Moreno, V., Nicholls, S. C., Hillman, Y., Davey, L. S., Tizard, M. L., Schwarz, R. T. et al. (1985). Primary structure of the precursor to the three major surface antigens of Plasmodium falciparum merozoites. Nature, London 317, 270–273.CrossRefGoogle Scholar
Holder, A. A., Sandhu, J. S., Hillman, Y., Davey, L. S., Nicholls, S. C., Cooper, H. and Lockyer, M. J. (1987). Processing of the precursor to the major merozoite surface antigens of Plasmodium falciparum. Parasitology 94, 199–208.CrossRefGoogle Scholar
Koussis, K., Withers-Martinez, C., Yeoh, S., Child, M., Hackett, F., Knuepfer, E., Juliano, L., Woehlbier, U., Bujard, H. and Blackman, M. J. (2009). A multifunctional serine protease primes the malaria parasite for red blood cell invasion. EMBO Journal 28, 725–735.CrossRefGoogle ScholarPubMed
Ling, I. T., Ogun, S. A. and Holder, A. A. (1994). Immunization against malaria with a recombinant protein. Parasite Immunology 16, 63–67.CrossRefGoogle ScholarPubMed
Lyon, J. A., Haynes, J. D., Diggs, C. L., Chulay, J. D., Haidaris, C. G. and Pratt-Rossiter, J. (1987). Monoclonal antibody characterization of the 195-kilodalton major surface glycoprotein of Plasmodium falciparum malaria schizonts and merozoites: identification of additional processed products and a serotype-restricted repetitive epitope. Journal of Immunology 138, 895–901.CrossRefGoogle Scholar
Majarian, W. R., Daly, T. M., Weidanz, W. P. and Long, C. A. (1984). Passive immunization against murine malaria with an IgG3 monoclonal antibody. Journal of Immunology 132, 3131–3137.CrossRefGoogle ScholarPubMed
McBride, J. S. and Heidrich, H. G. (1987). Fragments of the polymorphic Mr 185,000 glycoprotein from the surface of isolated Plasmodium falciparum merozoites form an antigenic complex. Molecular and Biochemical Parasitology 23, 71–84.CrossRefGoogle Scholar
McIntosh, R. S., Shi, J., Jennings, R. M., Chappel, J. C., de Koning-Ward, T. F., Smith, T., Green, J., van Egmond, M., Leusen, J. H., Lazarou, M., van de Winkel, M. J., Jones, T. S., Crabb, B. S., Holder, A. A. and Pleass, R. J. (2007). The importance of human FcgammaRI in mediating protection to malaria. PLoS Pathogens 3, e72.CrossRefGoogle ScholarPubMed
Morgan, W. D., Birdsall, B., Frenkiel, T. A., Gradwell, M. G., Burghaus, P. A., Syed, S. E., Uthaipibull, C., Holder, A. A. and Feeney, J. (1999). Solution structure of an EGF module pair from the Plasmodium falciparum merozoite surface protein 1. Journal of Molecular Biology 289, 113–122.CrossRefGoogle ScholarPubMed
Morgan, W. D., Frenkiel, T. A., Lock, M. J., Grainger, M. and Holder, A. A. (2005). Precise epitope mapping of malaria parasite inhibitory antibodies by TROSY NMR cross-saturation. Biochemistry 44, 518–523.CrossRefGoogle ScholarPubMed
Morgan, W. D., Lock, M. J., Frenkiel, T. A., Grainger, M. and Holder, A. A. (2004). Malaria parasite-inhibitory antibody epitopes on Plasmodium falciparum merozoite surface protein-1(19) mapped by TROSY NMR. Molecular and Biochemical Parasitology 138, 29–36.CrossRefGoogle Scholar
Murphy, V. F., Rowan, W. C., Page, M. J. and Holder, A. A. (1990). Expression of hybrid malaria antigens in insect cells and their engineering for correct folding and secretion. Parasitology 100, 177–183.CrossRefGoogle ScholarPubMed
Nwuba, R. I., Sodeinde, O., Anumudu, C. I., Omosun, Y. O., Odaibo, A. B., Holder, A. A. and Nwagwu, M. (2002). The human immune response to Plasmodium falciparum includes both antibodies that inhibit merozoite surface protein 1 secondary processing and blocking antibodies. Infection and Immunity 70, 5328–5331.CrossRefGoogle ScholarPubMed
O'Donnell, R. A., de Koning-Ward, T. F., Burt, R. A., Bockarie, M., Reeder, J. C., Cowman, A. F. and Crabb, B. S. (2001). Antibodies against merozoite surface protein (MSP)-1(19) are a major component of the invasion-inhibitory response in individuals immune to malaria. Journal of Experimental Medicine 193, 1403–1412.CrossRefGoogle Scholar
Ogun, S. A., Dumon-Seignovert, L., Marchand, J. B., Holder, A. A. and Hill, F. (2008). The oligomerization domain of C4-binding protein (C4bp) acts as an adjuvant, and the fusion protein comprised of the 19-kilodalton merozoite surface protein 1 fused with the murine C4bp domain protects mice against malaria. Infection and Immunity 76, 3817–3823.CrossRefGoogle ScholarPubMed
Ogutu, B. R., Apollo, O. J., McKinney, D., Okoth, W., Siangla, J., Dubovsky, F., Tucker, K., Waitumbi, J. N., Diggs, C., Wittes, J. et al. (2009). Blood stage malaria vaccine eliciting high antigen-specific antibody concentrations confers no protection to young children in Western Kenya. PLoS ONE 4, e4708.CrossRefGoogle ScholarPubMed
Okech, B. A., Corran, P. H., Todd, J., Joynson-Hicks, A., Uthaipibull, C., Egwang, T. G., Holder, A. A. and Riley, E. M. (2004). Fine specificity of serum antibodies to Plasmodium falciparum merozoite surface protein, PfMSP-1(19), predicts protection from malaria infection and high-density parasitemia. Infection and Immunity 72, 1557–1567.CrossRefGoogle ScholarPubMed
Omosun, Y. O., Adoro, S., Anumudu, C. I., Odaibo, A. B., Uthiapibull, C., Holder, A. A., Nwagwu, M. and Nwuba, R. I. (2008). Antibody specificities of children living in a malaria endemic area to inhibitory and blocking epitopes on MSP-1(19) of Plasmodium falciparum. Acta Tropica 109, 208–212.CrossRefGoogle Scholar
Pachebat, J. A., Kadekoppala, M., Grainger, M., Dluzewski, A. R., Gunaratne, R. S., Scott-Finnigan, T. J., Ogun, S. A., Ling, I. T., Bannister, L. H., Taylor, H. M., Mitchell, G. H. and Holder, A. A. (2007). Extensive proteolytic processing of the malaria parasite merozoite surface protein 7 during biosynthesis and parasite release from erythrocytes. Molecular and Biochemical Parasitology 151, 59–69.CrossRefGoogle ScholarPubMed
Pachebat, J. A., Ling, I. T., Grainger, M., Trucco, C., Howell, S., Fernandez-Reyes, D., Gunaratne, R. and Holder, A. A. (2001). The 22 kDa component of the protein complex on the surface of Plasmodium falciparum merozoites is derived from a larger precursor, merozoite surface protein 7. Molecular and Biochemical Parasitology 117, 83–89.CrossRefGoogle ScholarPubMed
Pattaradilokrat, S., Cheesman, S. J. and Carter, R. (2007). Linkage group selection: towards identifying genes controlling strain specific protective immunity in malaria. PLoS ONE 2, e857.CrossRefGoogle ScholarPubMed
Perkins, M. E. and Rocco, L. J. (1988). Sialic acid-dependent binding of Plasmodium falciparum merozoite surface antigen, Pf200, to human erythrocytes. Journal of Immunology 141, 3190–3196.CrossRefGoogle ScholarPubMed
Pizarro, J. C., Chitarra, V., Verger, D., Holm, I., Petres, S., Dartevelle, S., Nato, F., Longacre, S. and Bentley, G. A. (2003). Crystal structure of a Fab complex formed with PfMSP1-19, the C-terminal fragment of merozoite surface protein 1 from Plasmodium falciparum: a malaria vaccine candidate. Journal of Molecular Biology 328, 1091–1103.CrossRefGoogle ScholarPubMed
Pleass, R. J. and Holder, A. A. (2005). Opinion: antibody-based therapies for malaria. Nature Reviews Microbiology 3, 893–899.CrossRefGoogle ScholarPubMed
Pleass, R. J., Ogun, S. A., McGuinness, D. H., van de Winkel, J. G., Holder, A. A. and Woof, J. M. (2003). Novel antimalarial antibodies highlight the importance of the antibody Fc region in mediating protection. Blood 102, 4424–4430.CrossRefGoogle ScholarPubMed
Sanders, P. R., Cantin, G. T., Greenbaum, D. C., Gilson, P. R., Nebl, T., Moritz, R. L., Yates, J. R. 3rd, Hodder, A. N. and Crabb, B. S. (2007). Identification of protein complexes in detergent-resistant membranes of Plasmodium falciparum schizonts. Molecular and Biochemical Parasitology 154, 148–157.CrossRefGoogle ScholarPubMed
Shi, J., McIntosh, R. S. and Pleass, R. J. (2006). Antibody- and Fc-receptor-based therapeutics for malaria. Clinical Science (London) 110, 11–19.CrossRefGoogle ScholarPubMed
Spencer Valero, L. M., Ogun, S. A., Fleck, S. L., Ling, I. T., Scott-Finnigan, T. J., Blackman, M. J. and Holder, A. A. (1998). Passive immunization with antibodies against three distinct epitopes on Plasmodium yoelii merozoite surface protein 1 suppresses parasitemia. Infection and Immunity 66, 3925–3930.CrossRefGoogle ScholarPubMed
Tanabe, K., Mackay, M., Goman, M. and Scaife, J. G. (1987). Allelic dimorphism in a surface antigen gene of the malaria parasite Plasmodium falciparum. Journal of Molecular Biology 195, 273–287.CrossRefGoogle Scholar
Trucco, C., Fernandez-Reyes, D., Howell, S., Stafford, W. H., Scott-Finnigan, T. J., Grainger, M., Ogun, S. A., Taylor, W. R. and Holder, A. A. (2001). The merozoite surface protein 6 gene codes for a 36 kDa protein associated with the Plasmodium falciparum merozoite surface protein-1 complex. Molecular and Biochemical Parasitology 112, 91–101.CrossRefGoogle ScholarPubMed
Uthaipibull, C., Aufiero, B., Syed, S. E., Hansen, B., Guevara Patino, J. A., Angov, E., Ling, I. T., Fegeding, K., Morgan, W. D., Ockenhouse, C., Birdsall, B., Feeney, J., Lyon, J. A. and Holder, A. A. (2001). Inhibitory and blocking monoclonal antibody epitopes on merozoite surface protein 1 of the malaria parasite Plasmodium falciparum. Journal of Molecular Biology 307, 1381–1394.CrossRefGoogle ScholarPubMed
Woehlbier, U., Epp, C., Kauth, C. W., Lutz, R., Long, C. A., Coulibaly, B., Kouyate, B., Arevalo-Herrera, M., Herrera, S. and Bujard, H. (2006). Analysis of antibodies directed against merozoite surface protein 1 of the human malaria parasite Plasmodium falciparum. Infection and Immunity 74, 1313–1322.CrossRefGoogle ScholarPubMed