Multiple plasmodium falciparum merozoite surface protein 1 complexes mediate merozoite binding to human erythrocytes

Journal of Biological Chemistry

Volumn 291, Issue 14, 2016, Pages 7703-7715

  Lin, Clara S ^a,b   Uboldi, Alessandro D ^a   Epp, Christian ^c   Bujard, Hermann ^c   Tsuboi, Takafumi ^d   Czabotar, Peter E ^a,b   Cowman, X Alan F ^a,b  

^a WALTER AND ELIZA HALL INSTITUTE OF MEDICAL RESEARCH   (Australia)

^b UNIVERSITY OF MELBOURNE   (Australia)

^c UNIVERSITY OF HEIDELBERG   (Germany)

^d EHIME UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

BINS; PROTEINS;

HUMAN ERYTHROCYTES; IN-VITRO; MEROZOITE SURFACE PROTEINS; OVERLAPPING FUNCTIONS; PARASITE; PARASITE GROWTH; PLASMODIUM FALCIPARUM;

BLOOD;

MEROZOITE SURFACE PROTEIN 1; MEROZOITE SURFACE PROTEIN 3; MEROZOITE SURFACE PROTEIN 6; MEROZOITE SURFACE PROTEIN 7; MICROORGANISM PROTEIN; PROTEIN MSPDBL1; PROTEIN MSPDBL2; UNCLASSIFIED DRUG; MULTIPROTEIN COMPLEX;

ANTIPROTOZOAL ACTIVITY; ARTICLE; COMPLEX FORMATION; CONTROLLED STUDY; ERYTHROCYTE; HOST PARASITE INTERACTION; HUMAN; HUMAN CELL; IN VITRO STUDY; MEROZOITE; NONHUMAN; PLASMODIUM FALCIPARUM; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN PROCESSING; PROTEIN TARGETING; METABOLISM; PARASITOLOGY;

ERYTHROCYTES; HUMANS; MEROZOITE SURFACE PROTEIN 1; MEROZOITES; MULTIPROTEIN COMPLEXES; PLASMODIUM FALCIPARUM;

EID: 84964871259     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M115.698282     Document Type: Article

References (56)

1. Cowman, A. F., and Crabb, B. S. (2006) Invasion of red blood cells by malaria parasites. Cell 124, 755-766.
2. Gilson, P. R., Nebl, T., Vukcevic, D., Moritz, R. L., Sargeant, T., Speed, T. P., Schofield, L., and Crabb, B. S. (2006) Identification and stoichiometry of glycosylphosphatidylinositol-anchored membrane proteins of the human malaria parasite Plasmodium falciparum. Mol. Cell. Proteomics 5, 1286-1299.
3. 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. Mol. Biochem. Parasitol. 23, 71-84.
4. 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.
5. 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. Proc. Natl. Acad. Sci. U.S.A. 100, 5164-5169.
6. Baldwin, M. R., Li, X., Hanada, T., Liu, S. C., and Chishti, A. H. (2015) Merozoite surface protein 1 recognition of host glycophorin A mediates malaria parasite invasion of red blood cells. Blood 125, 2704-2711.
7. Harris, K. S., Casey, J. L., Coley, A. M., Masciantonio, R., Sabo, J. K., Keizer, D. W., Lee, E. F., McMahon, A., Norton, R. S., Anders, R. F., and Foley, M. (2005) Binding hot spot for invasion inhibitory molecules on Plasmodium falciparum apical membrane antigen 1. Infect. Immun. 73, 6981-6989.
8. 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. J. Exp. Med. 172, 379-382.
9. 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. Mol. Biochem. Parasitol. 49, 29-33.
10. Blackman, M. J., Whittle, H., and Holder, A. A. (1991) Processing of the Plasmodium falciparum major merozoite surface protein-1: identification of a 33-kilodalton secondary processing product which is shed prior to erythrocyte invasion. Mol. Biochem. Parasitol. 49, 35-44.
11. Blackman, M. J., and Holder, A. A. (1992) Secondary processing of the Plasmodium falciparum merozoite surface protein-1 (MSP1) by a calcium- dependent membrane-bound serine protease: shedding of MSP133 as a noncovalently associated complex with other fragments of the MSP1. Mol. Biochem. Parasitol. 50, 307-315.
12. Stafford, W. H., Blackman, M. J., Harris, A., Shai, S., Grainger, M., and Holder, A. A. (1994) N-terminal amino acid sequence of the Plasmodium falciparum merozoite surface protein-1 polypeptides. Mol. Biochem. Parasitol. 66, 157-160.
13. Stafford, W. H., Günder, B., Harris, A., Heidrich, H. G., Holder, A. A., and Blackman, M. J. (1996) A 22 kDa protein associated with the Plasmodium falciparum merozoite surface protein-1 complex. Mol. Biochem. Parasitol. 80, 159-169.
14. 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. Mol. Biochem. Parasitol. 112, 91-101.
15. 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. Mol. Biochem. Parasitol. 117, 83-89.
16. Kauth, C. W., Woehlbier, U., Kern, M., Mekonnen, Z., Lutz, R., Mücke, N., Langowski, J., and Bujard, H. (2006) Interactions between merozoite surface proteins 1, 6, and 7 of the malaria parasite Plasmodium falciparum. J. Biol. Chem. 281, 31517-31527.
17. Lin, C. S., Uboldi, A. D., Marapana, D., Czabotar, P. E., Epp, C., Bujard, H., Taylor, N. L., Perugini, M. A., Hodder, A. N., and Cowman, A. F. (2014) The merozoite surface protein 1 complex is a platform for binding to human erythrocytes by Plasmodium falciparum. J. Biol. Chem. 289, 25655-28669.
18. Kadekoppala, M., Ogun, S. A., Howell, S., Gunaratne, R. S., and Holder, A. A. (2010) Systematic genetic analysis of the Plasmodium falciparum MSP7-like family reveals differences in protein expression, location, and importance in asexual growth of the blood-stage parasite. Eukaryot. Cell 9, 1064-1074.
19. Hodder, A. N., Czabotar, P. E., Uboldi, A. D., Clarke, O. B., Lin, C. S., Healer, J., Smith, B. J., and Cowman, A. F. (2012) Insights into Duffy binding-like domains through the crystal structure and function of the merozoite surface protein MSPDBL2 from Plasmodium falciparum. J. Biol. Chem. 287, 32922-32939.
20. Rodríguez, L. E., Curtidor, H., Ocampo, M., Garcia, J., Puentes, A., Valbuena, J., Vera, R., López, R., and Patarroyo, M. E. (2005) Identifying Plasmodium falciparum merozoite surface antigen 3 (MSP3) protein peptides that bind specifically to erythrocytes and inhibit merozoite invasion. Protein Sci. 14, 1778-1786.
21. Woehlbier, U., Epp, C., Kauth, C. W., Lutz, R., Long, C. A., Coulibaly, B., Kouyaté, 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. Infect. Immun. 74, 1313-1322.
22. 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. J. Exp. Med. 193, 1403-1412.
23. Sakamoto, H., Takeo, S., Maier, A. G., Sattabongkot, J., Cowman, A. F., and Tsuboi, T. (2012) Antibodies against a Plasmodium falciparum antigen PfMSPDBL1 inhibit merozoite invasion into human erythrocytes. Vaccine 30, 1972-1980.
24. Chiu, C. Y., Hodder, A. N., Lin, C. S., Hill, D. L., Li Wai Suen, C. S., Schofield, L., Siba, P. M., Mueller, I., Cowman, A. F., and Hansen, D. S. (2015) Antibodies to the Plasmodium falciparum proteins MSPDBL1 and MSPDBL2 opsonize merozoites, inhibit parasite growth, and predict protection from clinical malaria. J. Infect. Dis. 212, 406-415.
25. Osier, F. H., Mackinnon, M. J., Crosnier, C., Fegan, G., Kamuyu, G., Wanaguru, M., Ogada, E., McDade, B., Rayner, J. C., Wright, G. J., and Marsh, K. (2014) New antigens for a multicomponent blood-stage malaria vaccine. Sci. Transl. Med. 6, 247ra102.
26. Bouharoun-Tayoun, H., Attanath, P., Sabchareon, A., Chongsuphajaisiddhi, T., and Druilhe P. (1990) Antibodies that protect humans against Plasmodium falciparum blood stages do not on their own inhibit parasite growth and invasion in vitro, but act in cooperation with monocytes. J. Exp. Med. 172, 1633-1641.
27. Oeuvray, C., Bouharoun-Tayoun, H., Gras-Masse, H., Bottius, E., Kaidoh, T., Aikawa, M., Filgueira, M. C., Tartar, A., and Druilhe, P. (1994) Merozoite surface protein-3: A malaria protein inducing antibodies that promote Plasmodium falciparum killing by cooperation with blood mono- cytes. Blood 84, 1594-1602.
28. Druilhe, P., Spertini, F., Soesoe, D., Corradin, G., Mejia, P., Singh, S., Audran, R., Bouzidi, A., Oeuvray, C., and Roussilhon, C. (2005) A malaria vaccine that elicits in humans antibodies able to kill Plasmodium falciparum. Plos Med. 2, e344.
29. Singh, S., Soe, S., Roussilhon, C., Corradin, G., and Druilhe, P. (2005) Plasmodium falciparum merozoite surface protein 6 displays multiple targets for naturally occurring antibodies that mediate monocyte-dependent parasite killing. Infect. Immun. 73, 1235-1238.
30. Singh, S., Soe, S., Weisman, S., Barnwell, J. W., Pérignon, J. L., and Druilhe, P. (2009) Aconserved multi-gene family induces cross-reactive antibodies effective in defense against Plasmodium falciparum. Plos One 4, e5410.
31. Tetteh, K. K., Stewart, L. B., Ochola, L. I., Amambua-Ngwa, A., Thomas, A. W., Marsh, K., Weedall, G. D., and Conway, D. J. (2009) Prospective identification of malaria parasite genes under balancing selection. Plos One 4, e5568.
32. Ochola, L. I., Tetteh, K. K., Stewart, L. B., Riitho, V., Marsh, K., and Conway, D. J. (2010) Allele frequency-based and polymorphism-versus-divergence indices of balancing selection in a new filtered set of polymorphic genes in Plasmodium falciparum. Mol. Biol. Evol. 27, 2344-2351.
33. Weedall, G. D., and Conway, D. J. (2010) Detecting signatures of balancing selection to identify targets of anti-parasite immunity. Trends Parasitol. 26, 363-369.
34. Amambua-Ngwa, A., Tetteh, K. K., Manske, M., Gomez-Escobar, N., Stewart, L. B., Deerhake, M. E., Cheeseman, I. H., Newbold, C. I., Holder, A. A., Knuepfer, E., Janha, O., Jallow, M., Campino, S., Macinnis, B., Kwiatkowski, D. P., et al. (2012) Population genomic scan for candidate signatures of balancing selection to guide antigen characterization in malaria parasites. Plos genet. 8, e1002992.
35. Van Tyne, D., Park, D. J., Schaffner, S. F., Neafsey, D. E., Angelino, E., Cortese, J. F., Barnes, K. G., Rosen, D. M., Lukens, A. K., Daniels, R. F., Milner, D. A. Jr., Johnson, C. A., Shlyakhter, I., Grossman, S. R., Becker, J. S., et al. (2011) Identification and functional validation of the novel antimalarial resistance locus PF10-0355 in Plasmodium falciparum. Plos Genet. 7, e1001383.
36. Mills, K. E., Pearce, J. A., Crabb, B. S., and Cowman, A. F. (2002) Truncation of merozoite surface protein 3 disrupts its trafficking and that of acidic-basic repeat protein to the surface of Plasmodium falciparum merozoites. Mol. Microbiol. 43, 1401-1411.
37. 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. Mol. Biochem. Parasitol. 151, 59-69.
38. Burgess, B. R., Schuck, P., and Garboczi, D. N. (2005) Dissection of merozoite surface protein 3, a representative of a family of Plasmodium falciparum surface proteins, reveals an oligomeric and highly elongated molecule. J. Biol. Chem. 280, 37236-37245.
39. Crewther, P. E., Culvenor, J. G., Silva, A., Cooper, J. A., and Anders, R. F. (1990) Plasmodium falciparum: Two antigens of similar size are located in different compartments of the rhoptry. Exp. Parasitol. 70, 193-206.
40. Narum, D. L., and Thomas, A. W. (1994) Differential localization of fulllength and processed forms of PF83/AMA-1 an apical membrane antigen of Plasmodium falciparum merozoites. Mol. Biochem. Parasitol. 67, 59-68.
41. Howell, S. A., Withers-Martinez, C., Kocken, C. H., Thomas, A. W., and Blackman, M. J. (2001) Proteolytic processing and primary structure of Plasmodium falciparum apical membrane antigen-1. J. Biol. Chem. 276, 31311-31320.
42. Blackman, M. J., Chappel, J. A., Shai, S., and Holder, A. A. (1993) A conserved parasite serine protease processes the Plasmodium falciparum merozoite surface protein-1. Mol. Biochem. Parasitol. 62, 103-114.
43. Sanders, P. R., Cantin, G. T., Greenbaum, D. C., Gilson, P. R., Nebl, T., Moritz, R. L., Yates, J. R., Hodder, A. N., and Crabb, B. S. (2007) Identification of protein complexes in detergent-resistant membranes of Plasmodium falciparum schizonts. Mol. Biochem. Parasitol. 154, 148 -157.
44. Sim, B. K., Carter, J. M., Deal, C. D., Holland, C., Haynes, J. D., and Gross, M. (1994) Plasmodium falciparum: further characterization of a functionally active region of the merozoite invasion ligand EBA-175. Exp. Parasitol. 78, 259-268.
45. Thompson, J. K., Triglia, T., Reed, M. B., and Cowman, A. F. (2001) A novel ligand from Plasmodium falciparum that binds to a sialic acidcontaining receptor on the surface of human erythrocytes. Mol. Microbiol. 41, 47-58.
46. Das, S., Hertrich, N., Perrin, A. J., Withers-Martinez, C., Collins, C. R., Jones, M. L., Watermeyer, J. M., Fobes, E. T., Martin, S. R., Saibil, H. R., Wright, G. J., Treeck, M., Epp, C., and Blackman, M. J. (2015) Processing of Plasmodium falciparum merozoite surface protein MSP1 activates a spectrin- binding function enabling parasite egress from RBCs. Cell Host Microbe 18, 433-444.
47. Li, X., Chen, H., Oo, T. H., Daly, T. M., Bergman, L. W., Liu, S. C., Chishti, A. H., and Oh, S. S. (2004) A co-ligand complex anchors Plasmodium falciparum merozoites to the erythrocyte invasion receptor band 3. J. Biol. Chem. 279, 5765-5771.
48. Blackman, M. J. (2004) Proteases in host cell invasion by the malaria parasite. Cell. Microbiol. 6, 893-903.
49. Moss, D. K., Remarque, E. J., Faber, B. W., Cavanagh, D. R., Arnot, D. E., Thomas, A. W., and Holder, A. A. (2012) Plasmodium falciparum 19- kilodalton merozoite surface protein 1 (MSP1)-specific antibodies that interfere with parasite growth in vitro can inhibit MSP1 processing, merozoite invasion, and intracellular parasite development. Infect. Immun. 80, 1280-1287.
50. Wickramarachchi, T., Cabrera, A. L., Sinha, D., Dhawan, S., Chandran, T., Devi, Y. S., Kono, M., Spielmann, T., Gilberger, T. W., Chauhan, V. S., and Mohmmed, A. (2009) A novel Plasmodium falciparum erythrocyte binding protein associated with the merozoite surface, PfDBLMSP. Int. J. Parasitol. 39, 763-773.
51. Campanale, N., Nickel, C., Daubenberger, C. A., Wehlan, D. A., Gorman, J. J., Klonis, N., Becker, K., and Tilley, L. (2003) Identification and characterization of heme-interacting proteins in the malaria parasite, Plasmodium falciparum. J. Biol. Chem. 278, 27354-27361.
52. Imam, M., Singh, S., Kaushik, N. K., and Chauhan, V. S. (2014) Plasmodium falciparum merozoite surface protein 3: oligomerization, self-assembly, and heme complex formation. J. Biol. Chem. 289, 3856-3868.
53. Reed, M. B., Caruana, S. R., Batchelor, A. H., Thompson, J. K., Crabb, B. S., and Cowman, A. F. (2000) Targeted disruption of an erythrocyte binding antigen in Plasmodium falciparum is associated with a switch toward a sialic acid independent pathway of invasion. Proc. Natl. Acad. Sci. U.S.A. 97, 7509-7514.
54. Duraisingh, M. T., Triglia, T., Ralph, S. A., Rayner, J. C., Barnwell, J. W., McFadden, G. I., and Cowman, A. F. (2003) Phenotypic variation of Plasmodium falciparum merozoite proteins directs receptor targeting for invasion of human erythrocytes. EMBO J. 22, 1047-1057.
55. Stubbs, J., Simpson, K. M., Triglia, T., Plouffe, D., Tonkin, C. J., Duraisingh, M. T., Maier, A. G., Winzeler, E. A., and Cowman, A. F. (2005) Molecular mechanism for switching of P. falciparum invasion pathways into human erythrocytes. Science 309, 1384-1387.
56. Gondeau, C., Corridin, G., Heitz, F., Le Peuch, C., Balbo, A., Schuck, P., and Kajava, A. V. (2009) The C-terminal domain of Plasmodium falciparum merozoite surface protein 3 self-assembles into alpha-helical coiledcoil tetramer. Mol. Biochem. Parasitol. 165, 153-161.