Plasmodium falciparum merozoite surface protein 3: Oligomerization, self-assembly, and heme complex formation

Journal of Biological Chemistry

Volumn 289, Issue 7, 2014, Pages 3856-3868

  Imam, Maryam ^a   Singh, Shailja ^a   Kaushik, Naveen Kumar ^a   Chauhan, Virander Singh ^a  

^a INTERNATIONAL CENTRE FOR GENETIC ENGINEERING AND BIOTECHNOLOGY   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

AMYLOID; ERYTHROCYTE; HEME; INFECTIOUS DISEASES; MALARIA;

ANTIGENS, PROTOZOAN; ERYTHROCYTES; HEME; HEMEPROTEINS; HUMANS; MALARIA, FALCIPARUM; PLASMODIUM FALCIPARUM; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, TERTIARY; PROTOZOAN PROTEINS; SCHIZONTS;

EID: 84894219942     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.520239     Document Type: Article

References (73)

1. Miller, L. H., Good, M. F., and Milon, G. (1994) Malaria pathogenesis. Science 264, 1878-1883
2. Chauhan, V. S., Yazdani, S. S., and Gaur, D. (2010) Malaria vaccine development based on merozoite surface proteins of Plasmodium falciparum. Hum. Vaccin. 6, 757-762
3. Schwartz, L., Brown, G. V., Genton, B., and Moorthy, V. S. (2012)Areview of malaria vaccine clinical projects based on the WHO rainbow table. Malar. J. 11, 11
4. Gaur, D., Mayer, D. C., and Miller, L. H. (2004) Parasite ligand-host receptor interactions during invasion of erythrocytes by Plasmodium merozoites. Int. J. Parasitol. 34, 1413-1429
5. 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 monocytes. Blood 84, 1594-1602
6. Singh, S., Soe, S., Mejia, J. P., Roussilhon, C., Theisen, M., Corradin, G., and Druilhe, P. (2004) Identification of a conserved region of Plasmodium falciparum MSP3 targeted by biologically active antibodies to improve vaccine design. J. Infect. Dis. 190, 1010-1018
7. 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
8. Hisaeda, H., Saul, A., Reece, J. J., Kennedy, M. C., Long, C. A., Miller, L. H., and Stowers, A. W. (2002) Merozoite surface protein 3 and protection against malaria in Aotus nancymai monkeys. J. Infect. Dis. 185, 657-664
9. Audran, R., Cachat, M., Lurati, F., Soe, S., Leroy, O., Corradin, G., Druilhe, P., and Spertini, F. (2005) Phase I malaria vaccine trial with a long synthetic peptide derived from the merozoite surface protein 3 antigen. Infect. Immun. 73, 8017-8026
10. Sirima, S. B., Nébié, I., Ouédraogo, A., Tiono, A. B., Konaté, A. T., Gansané, A., Dermé, A. I., Diarra, A., Ouédraogo, A., Soulama, I., Cuzzin-Ouattara, N., Cousens, S., and Leroy, O. (2007) Safety and immunogenicity of the Plasmodium falciparum merozoite surface protein-3 long synthetic peptide (MSP3-LSP) malaria vaccine in healthy, semi-immune adult males in Burkina Faso, West Africa. Vaccine 25, 2723-2732
11. Huy, N. T., Serada, S., Trang, D. T., Takano, R., Kondo, Y., Kanaori, K., Tajima, K., Hara, S., and Kamei, K. (2003) Neutralization of toxic heme by Plasmodium falciparum histidine-rich protein 2. J. Biochem. 133, 693-698
12. Francis, S. E., Sullivan, D. J., Jr., and Goldberg, D. E. (1997) Hemoglobin metabolism in the malaria parasite Plasmodium falciparum. Annu. Rev. Microbiol. 51, 97-123
13. Schneider, E. L., and Marletta, M. A. (2005) Heme binding to the histidinerich protein II from Plasmodium falciparum. Biochemistry 44, 979-986
14. Pagola, S., Stephens, P. W., Bohle, D. S., Kosar, A. D., and Madsen, S. K. (2000) The structure of malaria pigment-haematin. Nature 404, 307-310
15. Balla, J., Vercellotti, G. M., Jeney, V., Yachie, A., Varga, Z., Eaton, J. W., and Balla, G. (2005) Heme, heme oxygenase, and ferritin in vascular endothelial cell injury. Mol. Nutr. Food Res. 49, 1030-1043
16. 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
17. Choi, C. Y., Cerda, J. F., Chu, H. A., Babcock, G. T., and Marletta, M. A. (1999) Spectroscopic characterization of the heme-binding sites in Plasmodium falciparum histidine-rich protein 2. Biochemistry 38, 16916-16924
18. Spycher, C., Klonis, N., Spielmann, T., Kump, E., Steiger, S., Tilley, L., and Beck, H. P. (2003) MAHRP-1, a novel Plasmodium falciparum histidinerich protein, binds ferriprotoporphyrin IX and localizes to the Maurer's clefts. J. Biol. Chem. 278, 35373-35383
19. McColl, D. J., Silva, A., Foley, M., Kun, J. F., Favaloro, J. M., Thompson, J. K., Marshall, V. M., Coppel, R. L., Kemp, D. J., and Anders, R. F. (1994) Molecular variation in a novel polymorphic antigen associated with Plasmodium falciparum merozoites. Mol. Biochem. Parasitol. 68, 53-67
20. Imam, M., Devi, Y. S., Verma, A. K., and Chauhan, V. S. (2011) Comparative immunogenicities of full-length Plasmodium falciparum merozoite surface protein 3 and a 24-kilodalton N-terminal fragment. Clin. Vaccine Immunol. 18, 1221-1228
21. Wittig, I., Braun, H. P., and Schägger, H. (2006) Blue native PAGE. Nat. Protoc. 1, 418-428
22. Fernandez-Escamilla, A. M., Rousseau, F., Schymkowitz, J., and Serrano, L. (2004) Prediction of sequence-dependent and mutational effects on the aggregation of peptides and proteins. Nat. Biotechnol. 22, 1302-1306
23. Pathak, S., and Chauhan, V. S. (2011) Rationale-based, de novo design of dehydrophenylalanine-containing antibiotic peptides and systematic modification in sequence for enhanced potency. Antimicrob. Agents Chemother. 55, 2178-2188
24. Haynes, J. D., Diggs, C. L., Hines, F. A., and Desjardins, R. E. (1976) Culture of human malaria parasites Plasmodium falciparum. Nature 263, 767-769
25. Srinivasan, P., Beatty, W. L., Diouf, A., Herrera, R., Ambroggio, X., Moch, J. K., Tyler, J. S., Narum, D. L., Pierce, S. K., Boothroyd, J. C., Haynes, J. D., and Miller, L. H. (2011) Binding of Plasmodium merozoite proteins RON2 and AMA1 triggers commitment to invasion. Proc. Natl. Acad. Sci. U.S.A. 108, 13275-13280
26. Singh, S., Alam, M. M., Pal-Bhowmick, I., Brzostowski, J. A., and Chitnis, C. E. (2010) Distinct external signals trigger sequential release of apical organelles during erythrocyte invasion by malaria parasites. PLoS Pathog. 6, e1000746
27. Miller, L. H., Aikawa, M., Johnson, J. G., and Shiroishi, T. (1979) Interaction between cytochalasin B-treated malarial parasites and erythrocytes. Attachment and junction formation. J. Exp. Med. 149, 172-184
28. Persson, K. E., McCallum, F. J., Reiling, L., Lister, N. A., Stubbs, J., Cowman, A. F., Marsh, K., and Beeson, J. G. (2008) Variation in use of erythrocyte invasion pathways by Plasmodium falciparum mediates evasion of human inhibitory antibodies. J. Clin. Invest. 118, 342-351
29. Tham, W. H., Wilson, D. W., Reiling, L., Chen, L., Beeson, J. G., and Cowman, A. F. (2009) Antibodies to reticulocyte binding protein-like homologue 4 inhibit invasion of Plasmodium falciparum into human erythrocytes. Infect. Immun. 77, 2427-2435
30. Brandish, P. E., Buechler, W., and Marletta, M. A. (1998) Regeneration of the ferrous heme of soluble guanylate cyclase from the nitric oxide complex: acceleration by thiols and oxyhemoglobin. Biochemistry 37, 16898-16907
31. Baskakov, I. V. (2004) Autocatalytic conversion of recombinant prion proteins displays a species barrier. J. Biol. Chem. 279, 7671-7677
32. Hoshi, M., Sato, M., Matsumoto, S., Noguchi, A., Yasutake, K., Yoshida, N., and Sato, K. (2003) Spherical aggregates of-amyloid (amylospheroid) show high neurotoxicity and activate tau protein kinase I/glycogen synthase kinase-3'. Proc. Natl. Acad. Sci. U.S.A. 100, 6370-6375
33. Loria, P., Miller, S., Foley, M., and Tilley, L. (1999) Inhibition of the peroxidative degradation of haem as the basis of action of chloroquine and other quinoline antimalarials. Biochem. J. 339, 363-370
34. Lambert, M. P., Barlow, A. K., Chromy, B. A., Edwards, C., Freed, R., Liosatos, M., Morgan, T. E., Rozovsky, I., Trommer, B., Viola, K. L., Wals, P., Zhang, C., Finch, C. E., Krafft, G. A., and Klein, W. L. (1998) Diffusible, nonfibrillar ligands derived from Aβ1-42 are potent central nervous system neurotoxins. Proc. Natl. Acad. Sci. U.S.A. 95, 6448-6453
35. Friedrich, R. P., Tepper, K., Rönicke, R., Soom, M., Westermann, M., Reymann, K., Kaether, C., and Fändrich, M. (2010) Mechanism of amyloid plaque formation suggests an intracellular basis of A pathogenicity. Proc. Natl. Acad. Sci. U.S.A. 107, 1942-1947
36. Lundberg, K. M., Stenland, C. J., Cohen, F. E., Prusiner, S. B., and Millhauser, G. L. (1997) Kinetics and mechanism of amyloid formation by the prion protein H1 peptide as determined by time-dependent ESR. Chem. Biol. 4, 345-355
37. Naiki, H., and Gejyo, F. (1999) Kinetic analysis of amyloid fibril formation. Methods Enzymol. 309, 305-318
38. Wood, S. J., Wypych, J., Steavenson, S., Louis, J. C., Citron, M., and Biere, A. L. (1999)-Synuclein fibrillogenesis is nucleation-dependent. Implications for the pathogenesis of Parkinson's disease. J. Biol. Chem. 274, 19509-19512
39. Harper, J. D., and Lansbury, P. T., Jr. (1997) Models of amyloid seeding in Alzheimer's disease and scrapie: mechanistic truths and physiological consequences of the time-dependent solubility of amyloid proteins. Annu. Rev. Biochem. 66, 385-407
40. Gondeau, C., Corradin, 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-helical coiled coil tetramer. Mol. Biochem. Parasitol. 165, 153-161
41. Bannister, L. H., Butcher, G. A., and Mitchell, G. H. (1977) Recent advances in understanding the invasion of erythrocytes by merozoites of Plasmodium knowlesi. Bull. World Health Organ. 55, 163-169
42. Bannister, L. H., Mitchell, G. H., Butcher, G. A., Dennis, E. D., and Cohen, S. (1986) Structure and development of the surface coat of erythrocytic merozoites of Plasmodium knowlesi. Cell Tissue Res. 245, 281-290
43. Dworkin, M. (1999) Fibrils as extracellular appendages of bacteria: their role in contact-mediated cell-cell interactions in Myxococcus xanthus. BioEssays 21, 590-595
44. Saarimaa, C., Peltola, M., Raulio, M., Neu, T. R., Salkinoja-Salonen, M. S., and Neubauer, P. (2006) Characterization of adhesion threads of Deinococcus geothermalis as type IV pili. J. Bacteriol. 188, 7016-7021
45. Clark, M. E., Edelmann, R. E., Duley, M. L., Wall, J. D., and Fields, M. W. (2007) Biofilm formation in Desulfovibrio vulgaris Hildenborough is dependent upon protein filaments. Environ. Microbiol. 9, 2844-2854
46. Walker, J. R., Gnanam, A. J., Blinkova, A. L., Hermandson, M. J., Karymov, M. A., Lyubchenko, Y. L., Graves, P. R., Haystead, T. A., and Linse, K. D. (2007) Clostridium taeniosporum spore ribbon-like appendage structure, composition and genes. Mol. Microbiol. 63, 629-643
47. 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
48. Cowman, A. F., Berry, D., and Baum, J. (2012) The cellular and molecular basis for malaria parasite invasion of the human red blood cell. J. Cell Biol. 198, 961-971
49. Cowman, A. F., and Crabb, B. S. (2006) Invasion of red blood cells by malaria parasites. Cell 124, 755-766
50. Zhang, X., Adda, C. G., Low, A., Zhang, J., Zhang, W., Sun, H., Tu, X., Anders, R. F., and Norton, R. S. (2012) Role of the helical structure of the N-terminal region of Plasmodium falciparum merozoite surface protein 2 in fibril formation and membrane interaction. Biochemistry 51, 1380-1387
51. Low, A., Chandrashekaran, I. R., Adda, C. G., Yao, S., Sabo, J. K., Zhang, X., Soetopo, A., Anders, R. F., and Norton, R. S. (2007) Merozoite surface protein 2 of Plasmodium falciparum: expression, structure, dynamics, and fibril formation of the conserved N-terminal domain. Biopolymers 87, 12-22
52. Yang, X., Adda, C. G., MacRaild, C. A., Low, A., Zhang, X., Zeng, W., Jackson, D. C., Anders, R. F., and Norton, R. S. (2010) Identification of key residues involved in fibril formation by the conserved N-terminal region of Plasmodium falciparum merozoite surface protein 2 (MSP2). Biochimie 92, 1287-1295
53. Adda, C. G., Murphy, V. J., Sunde, M., Waddington, L. J., Schloegel, J., Talbo, G. H., Vingas, K., Kienzle, V., Masciantonio, R., Howlett, G. J., Hodder, A. N., Foley, M., and Anders, R. F. (2009) Plasmodium falciparum merozoite surface protein 2 is unstructured and forms amyloid-like fibrils. Mol. Biochem. Parasitol. 166, 159-171
54. Puentes, A., Ocampo, M., Rodríguez, L. E., Vera, R., Valbuena, J., Curtidor, H., García, J., López, R., Tovar, D., Cortes, J., Rivera, Z., and Patarroyo, M. E. (2005) Identifying Plasmodium falciparum merozoite surface protein-10 human erythrocyte specific binding regions. Biochimie 87, 461-472
55. 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
56. Kumar, S., and Bandyopadhyay, U. (2005) Free heme toxicity and its detoxification systems in human. Toxicol. Lett. 157, 175-188
57. Ponka, P. (1999) Cell biology of heme. Am. J. Med. Sci. 318, 241-256
58. Letarte, P. B., Lieberman, K., Nagatani, K., Haworth, R. A., Odell, G. B., and Duff, T. A. (1993) Hemin: levels in experimental subarachnoid hematoma and effects on dissociated vascular smooth-muscle cells. J. Neurosurg. 79, 252-255
59. Vincent, S. H. (1989) Oxidative effects of heme and porphyrins on proteins and lipids. Semin. Hematol. 26, 105-113
60. Suliman, H. B., Carraway, M. S., Velsor, L. W., Day, B. J., Ghio, A. J., and Piantadosi, C. A. (2002) Rapid mtDNA deletion by oxidants in rat liver mitochondria after hemin exposure. Free Radic. Biol. Med. 32, 246-256
61. Morgan, W. T. (1985) The histidine-rich glycoprotein of serum has a domain rich in histidine, proline, and glycine that binds heme and metals. Biochemistry 24, 1496-1501
62. Kühl, T., Wissbrock, A., Goradia, N., Sahoo, N., Galler, K., Neugebauer, U., Popp, J., Heinemann, S. H., Ohlenschläger, O., and Imhof, D. (2013) Analysis of Fe(III) heme binding to cysteine-containing heme-regulatory motifs in proteins. ACS Chem. Biol. 8, 1785-1793
63. Aft, R. L., and Mueller, G. C. (1984) Hemin-mediated oxidative degradation of proteins. J. Biol. Chem. 259, 301-305
64. Tsutsui, K., and Mueller, G. C. (1982) A protein with multiple hemebinding sites from rabbit serum. J. Biol. Chem. 257, 3925-3931
65. Summers, C. A., and Flowers, R. A., 2nd (2000) Protein renaturation by the liquid organic salt ethylammonium nitrate. Protein Sci. 9, 2001-2008
66. Pamplona, A., Ferreira, A., Balla, J., Jeney, V., Balla, G., Epiphanio, S., Chora, A., Rodrigues, C. D., Gregoire, I. P., Cunha-Rodrigues, M., Portugal, S., Soares, M. P., and Mota, M. M. (2007) Heme oxygenase-1 and carbon monoxide suppress the pathogenesis of experimental cerebral malaria. Nat. Med. 13, 703-710
67. Mashima, R., Tilley, L., Siomos, M. A., Papalexis, V., Raftery, M. J., and Stocker, R. (2002) Plasmodium falciparum histidine-rich protein-2 (PfHRP2) modulates the redox activity of ferri-protoporphyrin IX (FePPIX): peroxidase-like activity of the PfHRP2-FePPIX complex. J. Biol. Chem. 277, 14514-14520
68. Gebbink, M. F., Claessen, D., Bouma, B., Dijkhuizen, L., and Wösten, H. A. (2005) Amyloids-a functional coat for microorganisms. Nat. Rev. Microbiol. 3, 333-341
69. Austin, J. W., Sanders, G., Kay, W. W., and Collinson, S. K. (1998) Thin aggregative fimbriae enhance Salmonella enteritidis biofilm formation. FEMS Microbiol. Lett. 162, 295-301
70. Khodarahmi, R., Naderi, F., Mostafaie, A., and Mansouri, K. (2010) Heme, as a chaperone, binds to amyloid fibrils and forms peroxidase in vitro: possible evidence on critical role of non-specific peroxidase activity in neurodegenerative disease onset/progression using the-crystallin-based experimental system. Arch. Biochem. Biophys. 494, 205-215
71. Ravi, L. B., Poosala, S., Ahn, D., Chrest, F. J., Spangler, E. L., Jayakumar, R., Nagababu, E., Mohanty, J. G., Talan, M., Ingram, D. K., and Rifkind, J. M. (2005) Red cell interactions with amyloid-γ(1-40) fibrils in a murine model. Neurobiol. Dis. 19, 28-37
72. Murali, J., Koteeswari, D., Rifkind, J. M., and Jayakumar, R. (2003) Amyloid insulin interaction with erythrocytes. Biochem. Cell Biol. 81, 51-59
73. Atamna, H., and Boyle, K. (2006) Amyloid peptide binds with heme to form a peroxidase: relationship to the cytopathologies of Alzheimer's disease. Proc. Natl. Acad. Sci. U.S.A. 103, 3381-3386