Sex-partitioning of the Plasmodium falciparum stage V gametocyte proteome provides insight into falciparum-specific cell biology

Molecular and Cellular Proteomics

Volumn 13, Issue 10, 2014, Pages 2705-2724

  Tao, Dingyin ^a   Ubaida Mohien, Ceereena ^b   Mathias, Derrick K ^a   King, Jonas G ^a   Pastrana Mena, Rebecca ^a   Tripathi, Abhai ^a   Goldowitz, Ilana ^c   Graham, David R ^b   Moss, Eli ^d   Marti, Matthias ^c   Dinglasan, Rhoel R ^a  

^a JOHNS HOPKINS BLOOMBERG SCHOOL OF PUBLIC HEALTH   (United States)

^b JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c HARVARD SCHOOL OF PUBLIC HEALTH   (United States)

^d BROAD INSTITUTE OF MIT AND HARVARD   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PARASITE ANTIBODY; PROTEIN ANTIBODY; PROTEOME; PROTOZOAL PROTEIN;

ARTICLE; BIOINFORMATICS; CELL MATURATION; CONTROLLED STUDY; CYTOLOGY; DIVERSIFYING SELECTION; EVOLUTIONARY ADAPTATION; FEMALE; GAMETOCYTE; GENETIC COMPLEMENTATION; GENETIC CONSERVATION; MALE; MASS SPECTROMETRY; MOSQUITO; NONHUMAN; PLASMODIUM BERGHEI; PLASMODIUM FALCIPARUM; PROTEIN ANALYSIS; PROTEOMICS; SEX; ANIMAL; BIOLOGY; GENE EXPRESSION REGULATION; GROWTH, DEVELOPMENT AND AGING; LIFE CYCLE STAGE; METABOLISM; PROCEDURES; SEX DIFFERENCE;

PLASMODIUM FALCIPARUM;

ANIMALS; COMPUTATIONAL BIOLOGY; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; LIFE CYCLE STAGES; MALE; PLASMODIUM FALCIPARUM; PROTOZOAN PROTEINS; SEX FACTORS;

EID: 84907953648     PISSN: 15359476     EISSN: 15359484     Source Type: Journal    
DOI: 10.1074/mcp.M114.040956     Document Type: Article

References (55)

1. Babiker, H. A., Schneider, P., and Reece, S. E. (2008) Gametocytes: insights gained during a decade of molecular monitoring. Trends Parasitol. 24, 525-530
2. Alonso, P. L., Brown, G., Arevalo-Herrera, M., Binka, F., Chitnis, C., Collins, F., Doumbo, O. K., Greenwood, B., Hall, B. F., Levine, M. M., Mendis, K., Newman, R. D., Plowe, C. V., Rodriguez, M. H., Sinden, R., Slutsker, L., and Tanner, M. (2011) A research agenda to underpin malaria eradication. PLoS Med. 8, e1000406
3. malERA Consultative Group on Drugs. (2011) A research agenda for malaria eradication: drugs. PLoS Med. 8, e1000402
4. malERA Consultative Group on Vaccines. (2011) A research agenda for malaria eradication: vaccines. PLoS Med. 8, e1000398
5. Bousema, T., and Drakeley, C. (2011) Epidemiology and infectivity of Plasmodium falciparum and Plasmodium vivax gametocytes in relation to malaria control and elimination. Clin. Microbiol. Rev. 24, 377-410
6. Paul, R. E., Brockman, A., Price, R. N., Luxemburger, C., White, N. J., Looareesuwan, S., Nosten, F., and Day, K. P. (1999) Genetic analysis of Plasmodium falciparum infections on the north-western border of Thailand. Trans. R. Soc. Trop. Med. Hyg. 93, 587-593
7. Robert, V., Read, A. F., Essong, J., Tchuinkam, T., Mulder, B., Verhave, J. P., and Carnevale, P. (1996) Effect of gametocyte sex ratio on infectivity of Plasmodium falciparum to Anopheles gambiae. Trans. R. Soc. Trop. Med. Hyg. 90, 621-624
8. Silvestrini, F., Lasonder, E., Olivieri, A., Camarda, G., van Schaijk, B., Sanchez, M., Younis Younis, S., Sauerwein, R., and Alano, P. (2010) Protein export marks the early phase of gametocytogenesis of the human malaria parasite Plasmodium falciparum. Mol. Cell. Proteomics 9, 1437-1448
9. Florens, L., Washburn, M. P., Raine, J. D., Anthony, R. M., Grainger, M., Haynes, J. D., Moch, J. K., Muster, N., Sacci, J. B., Tabb, D. L., Witney, A. A., Wolters, D., Wu, Y., Gardner, M. J., Holder, A. A., Sinden, R. E., Yates, J. R., and Carucci, D. J. (2002) A proteomic view of the Plasmodium falciparum life cycle. Nature 419, 520-526
10. Hall, N., Karras, M., Raine, J. D., Carlton, J. M., Kooij, T. W., Berriman, M., Florens, L., Janssen, C. S., Pain, A., Christophides, G. K., James, K., Rutherford, K., Harris, B., Harris, D., Churcher, C., Quail, M. A., Ormond, D., Doggett, J., Trueman, H. E., Mendoza, J., Bidwell, S. L., Rajandream, M. A., Carucci, D. J., Yates, J. R., 3rd., Kafatos, F. C., Janse, C. J., Barrell, B., Turner, C. M., Waters, A. P., and Sinden, R. E. (2005) A comprehensive survey of the Plasmodium life cycle by genomic, transcriptomic, and proteomic analyses. Science 307, 82-86
11. Khan, S. M., Franke-Fayard, B., Mair, G. R., Lasonder, E., Janse, C. J., Mann, M., and Waters, A. P. (2005) Proteome analysis of separated male and female gametocytes reveals novel sex-specific Plasmodium biology. Cell 121, 675-687
12. Sinden, R. E. (2009) Malaria, sexual development, and transmission: retrospect and prospect. Parasitology 136, 1427-1434
13. Sinden, R. E., Carter, R., Drakeley, C., and Leroy, D. (2012) The biology of sexual development of Plasmodium: the design and implementation of transmission-blocking strategies. Malar. J. 11, 70
14. Ponnudurai, T., Meuwissen, J. H., Leeuwenberg, A. D., Verhave, J. P., and Lensen, A. H. (1982) The production of mature gametocytes of Plasmodium falciparum in continuous cultures of different isolates infective to mosquitoes. Trans. R. Soc. Trop. Med. Hyg. 76, 242-250
15. Fivelman, Q. L., McRobert, L., Sharp, S., Taylor, C. J., Saeed, M., Swales, C. A., Sutherland, C. J., and Baker, D. A. (2007) Improved synchronous production of Plasmodium falciparum gametocytes in vitro. Mol. Biochem. Parasitol. 154, 119-123
16. Edwards, N., Wu, X., and Tseng, C. (2009) An unsupervised, model-free, machine-learning combiner for peptide identifications from tandem mass spectra. Clin. Proteomics 5, 23-36
17. Perkins, D. N., Pappin, D. J., Creasy, D. M., and Cottrell, J. S. (1999) Probability-based protein identification by searching sequence databases using mass spectrometry data. Electrophoresis 20, 3551-3567
18. Geer, L. Y., Markey, S. P., Kowalak, J. A., Wagner, L., Xu, M., Maynard, D. M., Yang, X., Shi, W., and Bryant, S. H. (2004) Open mass spectrometry search algorithm. J. Proteome Res. 3, 958-964
19. Craig, R., and Beavis, R. C. (2004) TANDEM: matching proteins with tandem mass spectra. Bioinformatics 20, 1466-1467
20. MacLean, B., Eng, J. K., Beavis, R. C., and McIntosh, M. (2006) General framework for developing and evaluating database scoring algorithms using the TANDEM search engine. Bioinformatics 22, 2830-2832
21. Tabb, D. L., Fernando, C. G., and Chambers, M. C. (2007) MyriMatch: highly accurate tandem mass spectral peptide identification by multivariate hypergeometric analysis. J. Proteome Res. 6, 654-661
22. Tanner, S., Shu, H., Frank, A., Wang, L. C., Zandi, E., Mumby, M., Pevzner, P. A., and Bafna, V. (2005) InsPecT: Identification of posttranslationally modified peptides from tandem mass spectra. Anal. Chem. 77, 4626-4639
23. Kim, S., Gupta, N., and Pevzner, P. A. (2008) Spectral probabilities and generating functions of tandem mass spectra: A strike against decoy databases. J. Proteome Res. 7, 3354-3363
24. Elias, J. E., and Gygi, S. P. (2007) Target-decoy search strategy for increased confidence in large-scale protein identifications by mass spectrometry. Nat. Methods 4, 207-214
25. Ubaida Mohien, C., Hartler, J., Breitwieser, F., Rix, U., Remsing Rix, L., Winter, G. E., Thallinger, G. G., Bennett, K. L., Superti-Furga, G., Trajanoski, Z., and Colinge, J. (2010) MASPECTRAS 2: an integration and analysis platform for proteomic data. Proteomics 10, 2719-2722
26. Taylor, C. F., Paton, N. W., Lilley, K. S., Binz, P. A., Julian, R. K., Jr., Jones, A. R., Zhu, W., Apweiler, R., Aebersold, R., Deutsch, E. W., Dunn, M. J., Heck, A. J., Leitner, A., Macht, M., Mann, M., Martens, L., Neubert, T. A., Patterson, S. D., Ping, P., Seymour, S. L., Souda, P., Tsugita, A., Vandekerckhove, J., Vondriska, T. M., Whitelegge, J. P., Wilkins, M. R., Xenarios, I., Yates, J. R., 3rd, and Hermjakob, H. (2007) The minimum information about a proteomics experiment (MIAPE). Nat. Biotechnol. 25, 887-893
27. Vizcaino, J. A., Cote, R. G., Csordas, A., Dianes, J. A., Fabregat, A., Foster, J. M., Griss, J., Alpi, E., Birim, M., Contell, J., O'Kelly, G., Schoenegger, A., Ovelleiro, D., Perez-Riverol, Y., Reisinger, F., Rios, D., Wang, R., and Hermjakob, H. (2013) The PRoteomics IDEntifications (PRIDE) database and associated tools: status in 2013. Nucleic Acids Res. 41, D1063-D1069
28. Petersen, T. N., Brunak, S., von Heijne, G., and Nielsen, H. (2011) SignalP 4.0: discriminating signal peptides from transmembrane regions. Nat. Methods 8, 785-786
29. Krogh, A., Larsson, B., von Heijne, G., and Sonnhammer, E. L. (2001) Predicting transmembrane protein topology with a hidden markov model: application to complete genomes. J. Mol. Biol. 305, 567-580
30. Danecek, P., Auton, A., Abecasis, G., Albers, C. A., Banks, E., DePristo, M. A., Handsaker, R. E., Lunter, G., Marth, G. T., Sherry, S. T., McVean, G., Durbin, R., and 1000 Genomes Project Analysis Group. (2011) The variant call format and VCFtools. Bioinformatics 27, 2156-2158
31. Weir, B. S., and Cockerham, C. C. (1984) Estimating F-statistics for the analysis of population structure. Evolution 38, 1358-1370
32. Saha, S., and Raghava, G. P. (2007) Prediction methods for B-cell epitopes. Methods Mol. Biol. 409, 387-394
33. Kim, Y., Ponomarenko, J., Zhu, Z., Tamang, D., Wang, P., Greenbaum, J., Lundegaard, C., Sette, A., Lund, O., Bourne, P. E., Nielsen, M., and Peters, B. (2012) Immune epitope database analysis resource. Nucleic Acids Res. 40, W525-W530
34. Delemarre, B. J., and van der Kaay, H. J. (1979) Tropical malaria contracted the natural way in the Netherlands. Ned. Tijdschr. Geneeskd. 123, 1981-1982
35. Guinet, F., Dvorak, J. A., Fujioka, H., Keister, D. B., Muratova, O., Kaslow, D. C., Aikawa, M., Vaidya, A. B., and Wellems, T. E. (1996) A developmental defect in Plasmodium falciparum male gametogenesis. J. Cell Biol. 135, 269-278
36. Furuya, T., Mu, J., Hayton, K., Liu, A., Duan, J., Nkrumah, L., Joy, D. A., Fidock, D. A., Fujioka, H., Vaidya, A. B., Wellems, T. E., and Su, X. Z. (2005) Disruption of a Plasmodium falciparum gene linked to male sexual development causes early arrest in gametocytogenesis. Proc. Natl. Acad. Sci. U.S.A. 102, 16813-16818
37. Pradel, G. (2007) Proteins of the malaria parasite sexual stages: expression, function and potential for transmission blocking strategies. Parasitology, 1-19
38. Ubaida Mohien, C., Colquhoun, D. R., Mathias, D. K., Gibbons, J. G., Armistead, J. S., Rodriguez, M. C., Rodriguez, M. H., Edwards, N. J., Hartler, J., Thallinger, G. G., Graham, D. R., Martinez-Barnetche, J., Rokas, A., and Dinglasan, R. R. (2013) A bioinformatics approach for integrated transcriptomic and proteomic comparative analyses of model and nonsequenced anopheline vectors of human malaria parasites. Mol. Cell. Proteomics 12, 120-131
39. van Schaijk, B. C., van Dijk, M. R., van, d. V., van Gemert, G. J., van Dooren, M. W., Eksi, S., Roeffen, W. F., Janse, C. J., Waters, A. P., and Sauerwein, R. W. (2006) Pfs47, paralog of the male fertility factor Pfs48/45, is a female specific surface protein in Plasmodium falciparum. Mol. Biochem. Parasitol. 149, 216-222
40. 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
41. Lal, K., Delves, M. J., Bromley, E., Wastling, J. M., Tomley, F. M., and Sinden, R. E. (2009) Plasmodium male development gene-1 (mdv-1) is important for female sexual development and identifies a polarised plasma membrane during zygote development. Int. J. Parasitol. 39, 755-761
42. Ponzi, M., Siden-Kiamos, I., Bertuccini, L., Curra, C., Kroeze, H., Camarda, G., Pace, T., Franke-Fayard, B., Laurentino, E. C., Louis, C., Waters, A. P., Janse, C. J., and Alano, P. (2009) Egress of Plasmodium berghei gametes from their host erythrocyte is mediated by the MDV-1/PEG3 protein. Cell. Microbiol. 11, 1272-1288
43. Simon, N., Scholz, S. M., Moreira, C. K., Templeton, T. J., Kuehn, A., Dude, M. A., and Pradel, G. (2009) Sexual stage adhesion proteins form multiprotein complexes in the malaria parasite Plasmodium falciparum. J. Biol. Chem. 284, 14537-14546
44. 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., Yamins, D., Karlsson, E. K., Ndiaye, D., Sarr, O., Mboup, S., Happi, C., Furlotte, N. A., Eskin, E., Kang, H. M., Hartl, D. L., Birren, B. W., Wiegand, R. C., Lander, E. S., Wirth, D. F., Volkman, S. K., and Sabeti, P. C. (2011) Identification and functional validation of the novel antimalarial resistance locus PF10-0355 in Plasmodium falciparum. PLoS Genet. 7, e1001383
45. Reininger, L., Tewari, R., Fennell, C., Holland, Z., Goldring, D., Ranford-Cartwright, L., Billker, O., and Doerig, C. (2009) An essential role for the Plasmodium nek-2 nima-related protein kinase in the sexual development of malaria parasites. J. Biol. Chem. 284, 20858-20868
46. Mair, G. R., Braks, J. A., Garver, L. S., Wiegant, J. C., Hall, N., Dirks, R. W., Khan, S. M., Dimopoulos, G., Janse, C. J., and Waters, A. P. (2006) Regulation of sexual development of Plasmodium by translational repression. Science 313, 667-669
47. Molina-Cruz, A., Dejong, R. J., Ortega, C., Haile, A., Abban, E., Rodrigues, J., Jaramillo-Gutierrez, G., and Barillas-Mury, C. (2012) Some strains of Plasmodium falciparum, a human malaria parasite, evade the complement-like system of anopheles gambiae mosquitoes. Proc. Natl. Acad. Sci. U.S.A. 109, E1957-E1962
48. Manske, M., Miotto, O., Campino, S., Auburn, S., Almagro-Garcia, J., Maslen, G., O'Brien, J., Djimde, A., Doumbo, O., Zongo, I., Ouedraogo, J. B., Michon, P., Mueller, I., Siba, P., Nzila, A., Borrmann, S., Kiara, S. M., Marsh, K., Jiang, H., Su, X. Z., Amaratunga, C., Fairhurst, R., Socheat, D., Nosten, F., Imwong, M., White, N. J., Sanders, M., Anastasi, E., Alcock, D., Drury, E., Oyola, S., Quail, M. A., Turner, D. J., Ruano-Rubio, V., Jyothi, D., Amenga-Etego, L., Hubbart, C., Jeffreys, A., Rowlands, K., Sutherland, C., Roper, C., Mangano, V., Modiano, D., Tan, J. C., Ferdig, M. T., Amambua-Ngwa, A., Conway, D. J., Takala-Harrison, S., Plowe, C. V., Rayner, J. C., Rockett, K. A., Clark, T. G., Newbold, C. I., Berriman, M., MacInnis, B., and Kwiatkowski, D. P. (2012) Analysis of Plasmodium falciparum diversity in natural infections by deep sequencing. Nature 487, 375-379
49. Anthony, T. G., Polley, S. D., Vogler, A. P., and Conway, D. J. (2007) Evidence of nonneutral polymorphism in Plasmodium falciparum gamete surface protein genes Pfs47 and Pfs48/45. Mol. Biochem. Parasitol. 156, 117-123
50. Joice, R., Narasimhan, V., Montgomery, J., Sidhu, A. B., Oh, K., Meyer, E., Pierre-Louis, W., Seydel, K., Milner, D., Williamson, K., Wiegand, R., Ndiaye, D., Daily, J., Wirth, D., Taylor, T., Huttenhower, C., and Marti, M. (2013) Inferring developmental stage composition from gene expression in human malaria. PLoS Comput. Biol. 9, e1003392
51. Aingaran, M., Zhang, R., Law, S. K., Peng, Z., Undisz, A., Meyer, E., Diez-Silva, M., Burke, T. A., Spielmann, T., Lim, C. T., Suresh, S., Dao, M., and Marti, M. (2012) Host cell deformability is linked to transmission in the human malaria parasite Plasmodium falciparum. Cell. Microbiol. 14, 983-993
52. Florens, L., Liu, X., Wang, Y., Yang, S., Schwartz, O., Peglar, M., Carucci, D. J., Yates, J. R., 3rd, and Wub, Y. (2004) Proteomics approach reveals novel proteins on the surface of malaria-infected erythrocytes. Mol. Biochem. Parasitol. 135, 1-11
53. Trieu, A., Kayala, M. A., Burk, C., Molina, D. M., Freilich, D. A., Richie, T. L., Baldi, P., Felgner, P. L., and Doolan, D. L. (2011) Sterile protective immunity to malaria is associated with a panel of novel P. falciparum antigens. Mol. Cell. Proteomics 10, M111.007948
54. Ecker, A., Bushell, E. S., Tewari, R., and Sinden, R. E. (2008) Reverse genetics screen identifies six proteins important for malaria development in the mosquito. Mol. Microbiol. 70, 209-220
55. Carter, R., and Graves, P. M. (1988) Gametocytes. In Malaria: Principles and Practice of Malariology, 253-305