Structural and biochemical characterization of Plasmodium falciparum 12 (Pf12) reveals a unique interdomain organization and the potential for an antiparallel arrangement with Pf41

Journal of Biological Chemistry

Volumn 288, Issue 18, 2013, Pages 12805-12817

  Tonkin, Michelle L ^a   Arredondo, Silvia A ^b   Loveless, Bianca C ^a   Serpa, Jason J ^c   Makepeace, Karl A T ^c   Sundar, Natarajan ^b   Petrotchenko, Evgeniy V ^c   Miller, Louis H ^b   Grigg, Michael E ^b   Boulanger, Martin J ^a  

^a UNIVERSITY OF VICTORIA   (Canada)

^b NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

^c UNIVERSITY OF VICTORIA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIGENS; LIFE CYCLE; MASS SPECTROMETRY; PROTEINS;

BIOCHEMICAL CHARACTERIZATION; DOMAIN-CONTAINING PROTEINS; FUNCTIONAL DIVERSITY; FUNCTIONAL PROPERTIES; HETERODIMERIC COMPLEXES; INFECTED PATIENTS; PLASMODIUM FALCIPARUM; TOXOPLASMA GONDII;

CRYSTAL STRUCTURE;

CYSTEINE; HETERODIMER; MICROORGANISM PROTEIN; PLASMODIUM FALCIPARUM 12 PROTEIN; PLASMODIUM FALCIPARUM 41 PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; BIOCHEMISTRY; CELL ADHESION; CELL MEMBRANE; CONTROLLED STUDY; CRYSTAL STRUCTURE; HOST CELL; HOST PARASITE INTERACTION; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PURIFICATION; PROTEIN STRUCTURE; SCHIZONT; STRUCTURAL HOMOLOGY; STRUCTURE ANALYSIS; TOXOPLASMA GONDII;

EID: 84877115481     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.455667     Document Type: Article

References (68)

1. World Health Organization. (2010) World Malaria Report, World Health Organization, Geneva, Switzerland
2. Murray, C. J., Rosenfeld, L. C., Lim, S. S., Andrews, K. G., Foreman, K. J., Haring, D., Fullman, N., Naghavi, M., Lozano, R., and Lopez, A. D. (2012) Global malaria mortality between 1980 and 2010. A systematic analysis. Lancet 379, 413-431
3. Williamson, K. C., Criscio, M. D., and Kaslow, D. C. (1993) Cloning and expression of the gene for Plasmodium falciparum transmission-blocking target antigen, Pfs230. Mol. Biochem. Parasitol. 58, 355-358
4. Gerloff, D. L., Creasey, A., Maslau, S., and Carter, R. (2005) Structural models for the protein family characterized by gamete surface protein Pfs230 of Plasmodium falciparum. Proc. Natl. Acad. Sci. U.S.A. 102, 13598-13603 (Pubitemid 41420894)
5. Arredondo, S. A., Cai, M., Takayama, Y., MacDonald, N. J., Anderson, D. E., Aravind, L., Clore, G. M., and Miller, L. H. (2012) Structure of the Plasmodium 6-Cysteine s48/45 domain. Proc. Natl. Acad. Sci. U.S.A. 109, 6692-6697
6. van Dijk, M. R., Janse, C. J., Thompson, J., Waters, A. P., Braks, J. A., Dodemont, H. J., Stunnenberg, H. G., van Gemert, G. J., Sauerwein, R. W., and Eling, W. (2001) A central role for P48/45 in malaria parasite male gamete fertility. Cell 104, 153-164 (Pubitemid 32144980)
7. Kumar, N. (1987) Target antigens of malaria transmission-blocking immunity exist as a stable membrane-bound complex. Parasite Immunol. 9, 321-335
8. Williamson, K. C. (2003) Pfs230. From malaria transmission-blocking vaccine candidate toward function. Parasite Immunol. 25, 351-359
9. Eksi, S., Czesny, B., van Gemert, G. J., Sauerwein, R. W., Eling, W., and Williamson, K. C. (2006) Malaria transmission-blocking antigen, Pfs230, mediates human red blood cell binding to exflagellating male parasites and oocyst production. Mol. Microbiol. 61, 991-998 (Pubitemid 44134175)
10. van Schaijk, B. C., Janse, C. J., van Gemert, G. J., van Dijk, M. R., Gego, A., Franetich, J. F., van de Vegte-Bolmer, M., Yalaoui, S., Silvie, O., Hoffman, S. L., Waters, A. P., Mazier, D., Sauerwein, R. W., and Khan, S. M. (2008) Gene disruption of Plasmodium falciparum p52 results in attenuation of malaria liver stage development in cultured primary human hepatocytes. PLoS One 3, e3549
11. VanBuskirk, K. M., O'Neill, M. T., De La Vega, P., Maier, A. G., Krzych, U., Williams, J., Dowler, M. G., Sacci, J. B., Jr., Kangwanrangsan, N., Tsuboi, T., Kneteman, N. M., Heppner, D. G., Jr., Murdock, B. A., Mikolajczak, S. A., Aly, A. S., Cowman, A. F., and Kappe, S. H. (2009) Preerythrocytic, live-attenuated Plasmodium falciparum vaccine candidates by design. Proc. Natl. Acad. Sci. U.S.A. 106, 13004-13009
12. Chowdhury, D. R., Angov, E., Kariuki, T., and Kumar, N. (2009) A potent malaria transmission blocking vaccine based on codon harmonized full-length Pfs48/45 expressed in Escherichia coli. PLoS One 4, e6352
13. Quakyi, I. A., Carter, R., Rener, J., Kumar, N., Good, M. F., and Miller, L. H. (1987) The 230-kDa gamete surface protein of Plasmodium falciparum is also a target for transmission-blocking antibodies. J. Immunol. 139, 4213-4217 (Pubitemid 18013722)
14. van Dijk, M. R., Douradinha, B., Franke-Fayard, B., Heussler, V., van Dooren, M. W., van Schaijk, B., van Gemert, G. J., Sauerwein, R. W., Mota, M. M., Waters, A. P., and Janse, C. J. (2005) Genetically attenuated, P36p-deficient malarial sporozoites induce protective immunity and apoptosis of infected liver cells. Proc. Natl. Acad. Sci. U.S.A. 102, 12194-12199 (Pubitemid 41291151)
15. Waters, A. (2006) Malaria. New vaccines for old? Cell 124, 689-693
16. van Schaijk, B. C., Vos, M. W., Janse, C. J., Sauerwein, R. W., and Khan, S. M. (2010) Removal of heterologous sequences from Plasmodium falciparum mutants using FLPe-recombinase. PLoS One 5, e15121
17. Sanders, P. R., Gilson, P. R., Cantin, G. T., Greenbaum, D. C., Nebl, T., Carucci, D. J., McConville, M. J., Schofield, L., Hodder, A. N., Yates, J. R., 3rd, and Crabb, B. S. (2005) Distinct protein classes including novel merozoite surface antigens in Raft-like membranes of Plasmodium falciparum. J. Biol. Chem. 280, 40169-40176 (Pubitemid 41779153)
18. Elliott, J. F., Albrecht, G. R., Gilladoga, A., Handunnetti, S. M., Neequaye, J., Lallinger, G., Minjas, J. N., and Howard, R. J. (1990) Genes for Plasmodium falciparum surface antigens cloned by expression in COS cells. Proc. Natl. Acad. Sci. U.S.A. 87, 6363-6367
19. Reeder, J. C., Wapling, J., Mueller, I., Siba, P. M., and Barry, A. E. (2011) Population genetic analysis of the Plasmodium falciparum 6-Cys protein Pf38 in Papua New Guinea reveals domain-specific balancing selection. Malar. J. 10, 126
20. 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 (Pubitemid 44103399)
21. Taechalertpaisarn, T., Crosnier, C., Bartholdson, S. J., Hodder, A. N., Thompson, J., Bustamante, L. Y., Wilson, D. W., Sanders, P. R., Wright, G. J., Rayner, J. C., Cowman, A. F., Gilson, P. R., and Crabb, B. S. (2012) Biochemical and functional analysis of two Plasmodium falciparum blood-stage 6-Cys proteins. P12 and P41. PLoS One 7, e41937
22. Kumar, N., and Wizel, B. (1992) Further characterization of interactions between gamete surface antigens of Plasmodium falciparum. Mol. Biochem. Parasitol. 53, 113-120
23. Crawford, J., Grujic, O., Bruic, E., Czjzek, M., Grigg, M. E., and Boulanger, M. J. (2009) Structural characterization of the bradyzoite surface antigen (BSR4) from Toxoplasma gondii, a unique addition to the surface antigen glycoprotein 1-related superfamily. J. Biol. Chem. 284, 9192-9198
24. Crawford, J., Lamb, E., Wasmuth, J., Grujic, O., Grigg, M. E., and Boulanger, M. J. (2010) Structural and functional characterization of Sporo-SAG. A SAG2-related surface antigen from Toxoplasma gondii. J. Biol. Chem. 285, 12063-12070
25. He, X. L., Grigg, M. E., Boothroyd, J. C., and Garcia, K. C. (2002) Structure of the immunodominant surface antigen from the Toxoplasma gondii SRS superfamily. Nat. Struct. Biol. 9, 606-611 (Pubitemid 34816142)
26. Boulanger, M. J., Tonkin, M. L., and Crawford, J. (2010) Apicomplexan parasite adhesins. Novel strategies for targeting host cell carbohydrates. Curr. Opin. Struct. Biol. 20, 551-559
27. Wasmuth, J. D., Pszenny, V., Haile, S., Jansen, E. M., Gast, A. T., Sher, A., Boyle, J. P., Boulanger, M. J., Parkinson, J., and Grigg, M. E. (2012) Integrated bioinformatics and targeted deletion analyses of the SRS gene superfamily identify SRS29C as a negative regulator of Toxoplasma virulence. MBio 3, e00321-12
28. Aurrecoechea, C., Brestelli, J., Brunk, B. P., Dommer, J., Fischer, S., Gajria, B., Gao, X., Gingle, A., Grant, G., Harb, O. S., Heiges, M., Innamorato, F., Iodice, J., Kissinger, J. C., Kraemer, E., Li, W., Miller, J. A., Nayak, V., Pennington, C., Pinney, D. F., Roos, D. S., Ross, C., Stoeckert, C. J., Jr., Treatman, C., and Wang, H. (2009) PlasmoDB. A functional genomic database for malaria parasites. Nucleic Acids Res. 37, D539-D543
29. Massingham, T., and Goldman, N. (2005) Detecting amino acid sites under positive selection and purifying selection. Genetics 169, 1753-1762 (Pubitemid 40547480)
30. Sievers, F., Wilm, A., Dineen, D., Gibson, T. J., Karplus, K., Li, W., Lopez, R., McWilliam, H., Remmert, M., Söding, J., Thompson, J. D., and Higgins, D. G. (2011) Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal omega. Mol. Syst. Biol. 7, 539
31. Waterhouse, A. M., Procter, J. B., Martin, D. M., Clamp, M., and Barton, G. J. (2009) Jalview Version 2. A multiple sequence alignment editor and analysis workbench. Bioinformatics 25, 1189-1191
32. Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M., and Kumar, S. (2011) MEGA5. Molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol. Biol. Evol. 28, 2731-2739
33. Alexander, D. L., Arastu-Kapur, S., Dubremetz, J. F., and Boothroyd, J. C. (2006) Plasmodium falciparum AMA1 binds a rhoptry neck protein homologous to TgRON4, a component of the moving junction in Toxoplasma gondii. Eukaryot. Cell 5, 1169-1173 (Pubitemid 44100714)
34. Leslie, A. G. W. (1992) Joint CCP4 + ESF-EAMCB Newsletter on Protein Crystallography No. 26
35. Evans, P. (2006) Scaling and assessment of data quality. Acta Crystallogr.D Biol. Crystallogr. 62, 72-82
36. Winn, M. D., Ballard, C. C., Cowtan, K. D., Dodson, E. J., Emsley, P., Evans, P. R., Keegan, R. M., Krissinel, E. B., Leslie, A. G., McCoy, A., McNicholas, S. J., Murshudov, G. N., Pannu, N. S., Potterton, E. A., Powell, H. R., Read, R. J., Vagin, A., and Wilson, K. S. (2011) Overview of the CCP4 suite and current developments. Acta Crystallogr. D Biol. Crystallogr. 67, 235-242
37. McCoy, A. J., Grosse-Kunstleve, R. W., Adams, P. D., Winn, M. D., Storoni, L. C., and Read, R. J. (2007) Phaser crystallographic software. J. Appl. Crystallogr. 40, 658-674 (Pubitemid 47080256)
38. Schwarzenbacher, R., Godzik, A., Grzechnik, S. K., and Jaroszewski, L. (2004) The importance of alignment accuracy for molecular replacement. Acta Crystallogr. D Biol. Crystallogr. 60, 1229-1236 (Pubitemid 41073183)
39. Emsley, P., and Cowtan, K. (2004) Coot. Model-building tools for molecular graphics. Acta Crystallogr. D Biol. Crystallogr. 60, 2126-2132 (Pubitemid 41742764)
40. Murshudov, G. N., Vagin, A. A., and Dodson, E. J. (1997) Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr. D Biol. Crystallogr. 53, 240-255 (Pubitemid 27235885)
41. Petrotchenko, E. V., Serpa, J. J., Hardie, D. B., Berjanskii, M., Suriyamongkol, B. P., Wishart, D. S., and Borchers, C. H. (2012) Use of proteinase K nonspecific digestion for selective and comprehensive identification of interpeptide cross-links. application to prion proteins. Mol. Cell. Proteomics 11, M111.013524
42. Petrotchenko, E. V., and Borchers, C. H. (2010) ICC-CLASS. Isotopically coded cleavable cross-linking analysis software suite. BMC Bioinformatics 11, 64
43. Edgar, R. C. (2004) MUSCLE. Multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 32, 1792-1797
44. Eswar, N., Webb, B., Marti-Renom, M. A., Madhusudhan, M. S., Eramian, D., Shen, M. Y., Pieper, U., and Sali, A. (2006) Comparative protein structure modeling using Modeller. Curr. Protoc. Bioinformatics Chapter 5, Unit 5.6
45. Pettersen, E. F., Goddard, T. D., Huang, C. C., Couch, G. S., Greenblatt, D. M., Meng, E. C., and Ferrin, T. E. (2004) UCSF Chimera.Avisualization system for exploratory research and analysis. J. Comput. Chem. 25, 1605-1612
46. Polley, S. D., and Conway, D. J. (2001) Strong diversifying selection on domains of the Plasmodium falciparum apical membrane antigen 1 gene. Genetics 158, 1505-1512
47. 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
48. Beeson, J. G., Andrews, K. T., Boyle, M., Duffy, M. F., Choong, E. K., Byrne, T. J., Chesson, J. M., Lawson, A. M., and Chai, W. (2007) Structural basis for binding of Plasmodium falciparum erythrocyte membrane protein 1 to chondroitin sulfate and placental tissue and the influence of protein polymorphisms on binding specificity. J. Biol. Chem. 282, 22426-22436 (Pubitemid 47267337)
49. Tanabe, K., Escalante, A., Sakihama, N., Honda, M., Arisue, N., Horii, T., Culleton, R., Hayakawa, T., Hashimoto, T., Longacre, S., Pathirana, S., Handunnetti, S., and Kishino, H. (2007) Recent independent evolution of msp1 polymorphism in Plasmodium vivax and related simian malaria parasites. Mol. Biochem. Parasitol. 156, 74-79 (Pubitemid 47348140)
50. Williamson, K. C., and Kaslow, D. C. (1993) Strain polymorphism of Plasmodium falciparum transmission-blocking target antigen Pfs230. Mol. Biochem. Parasitol. 62, 125-127 (Pubitemid 223039544)
51. Anthony, T. G., Polley, S. D., Vogler, A. P., and Conway, D. J. (2007) Evidence of non-neutral polymorphism in Plasmodium falciparum gamete surface protein genes Pfs47 and Pfs48/45. Mol. Biochem. Parasitol. 156, 117-123 (Pubitemid 47600363)
52. Escalante, A. A., Grebert, H. M., Chaiyaroj, S. C., Riggione, F., Biswas, S., Nahlen, B. L., and Lal, A. A. (2002) Polymorphism in the gene encoding the Pfs48/45 antigen of Plasmodium falciparum. XI. Asembo Bay Cohort Project. Mol. Biochem. Parasitol. 119, 17-22 (Pubitemid 34038021)
53. van Dijk, M. R., van Schaijk, B. C., Khan, S. M., van Dooren, M. W., Ramesar, J., Kaczanowski, S., van Gemert, G. J., Kroeze, H., Stunnenberg, H. G., Eling, W. M., Sauerwein, R. W., Waters, A. P., and Janse, C. J. (2010) Three members of the 6-Cys protein family of Plasmodium play a role in gamete fertility. PLoS Pathog. 6, e1000853
54. Escalante, A. A., Lal, A. A., and Ayala, F. J. (1998) Genetic polymorphism and natural selection in the malaria parasite Plasmodium falciparum. Genetics 149, 189-202
55. 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
56. Li, J., Ito, D., Chen, J. H., Lu, F., Cheng, Y., Wang, B., Ha, K. S., Cao, J., Torii, M., Sattabongkot, J., Tsuboi, T., and Han, E. T. (2012) Pv12, a 6-Cys antigen of Plasmodium vivax, is localized to the merozoite rhoptry. Parasitol. Int. 61, 443-449
57. Moreno-Pérez, D. A., Areiza-Rojas, R., Flórez-Buitrago, X., Silva, Y., Patarroyo, M. E., and Patarroyo, M. A. (2013) The GPI-anchored 6-Cys protein Pv12 is present in detergent-resistant microdomains of Plasmodium vivax blood stage schizonts. Protist 164, 37-48
58. Williamson, K. C., Keister, D. B., Muratova, O., and Kaslow, D. C. (1995) Recombinant Pfs230, a Plasmodium falciparum gametocyte protein, induces antisera that reduce the infectivity of Plasmodium falciparum to mosquitoes. Mol. Biochem. Parasitol. 75, 33-42 (Pubitemid 26025504)
59. Outchkourov, N. S., Roeffen, W., Kaan, A., Jansen, J., Luty, A., Schuiffel, D., van Gemert, G. J., van de Vegte-Bolmer, M., Sauerwein, R. W., and Stunnenberg, H. G. (2008) Correctly folded Pfs48/45 protein of Plasmodium falciparum elicits malaria transmission-blocking immunity in mice. Proc. Natl. Acad. Sci. U.S.A. 105, 4301-4305 (Pubitemid 351754375)
60. Davidson, E. A., and Gowda, D. C. (2001) Glycobiology of Plasmodium falciparum. Biochimie 83, 601-604 (Pubitemid 32821223)
61. Krissinel, E., and Henrick, K. (2007) Inference of macromolecular assemblies from crystalline state. J. Mol. Biol. 372, 774-797 (Pubitemid 47321791)
62. Carter, R., Coulson, A., Bhatti, S., Taylor, B. J., and Elliott, J. F. (1995) Predicted disulfide-bonded structures for three uniquely related proteins of Plasmodium falciparum, Pfs230, Pfs48/45, and Pf12. Mol. Biochem. Parasitol. 71, 203-210
63. Holm, L., and Park, J. (2000) DaliLite workbench for protein structure comparison. Bioinformatics 16, 566-567
64. Cesbron-Delauw, M. F., Tomavo, S., Beauchamps, P., Fourmaux, M. P., Camus, D., Capron, A., and Dubremetz, J. F. (1994) Similarities between the primary structures of two distinct major surface proteins of Toxoplasma gondii. J. Biol. Chem. 269, 16217-16222 (Pubitemid 24209314)
65. Lekutis, C., Ferguson, D. J., and Boothroyd, J. C. (2000) Toxoplasma gondii. Identification of a developmentally regulated family of genes related to SAG2. Exp. Parasitol. 96, 89-96
66. Lekutis, C., Ferguson, D. J., Grigg, M. E., Camps, M., and Boothroyd, J. C. (2001) Surface antigens of Toxoplasma gondii. Variations on a theme. Int. J. Parasitol. 31, 1285-1292 (Pubitemid 32868708)
67. Jung, C., Lee, C. Y., and Grigg, M. E. (2004) The SRS superfamily of Toxoplasma surface proteins. Int. J. Parasitol. 34, 285-296 (Pubitemid 38299179)
68. Boothroyd, J. C., Hehl, A., Knoll, L. J., and Manger, I. D. (1998) The surface of Toxoplasma. More and less. Int. J. Parasitol. 28, 3-9