Integrated transcriptomic and proteomic analyses of P. Falciparum gametocytes: Molecular insight into sex-specific processes and translational repression

Nucleic Acids Research

Volumn 44, Issue 13, 2016, Pages 6087-6101

  Lasonder, Edwin ^a   Rijpma, Sanna R ^b   Van Schaijk, Ben C L ^b,c   Hoeijmakers, Wieteke A M ^c   Kensche, Philip R ^c   Gresnigt, Mark S ^b   Italiaander, Annet ^b   Vos, Martijn W ^b   Woestenenk, Rob ^b   Bousema, Teun ^b   Mair, Gunnar R ^d   Khan, Shahid M ^e   Janse, Chris J ^e   Bártfai, Richárd ^c   Sauerwein, Robert W ^b  

^a UNIVERSITY OF PLYMOUTH   (United Kingdom)

^b RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

^c RADBOUD UNIVERSITY NIJMEGEN   (Netherlands)

^d UNIVERSITY OF HEIDELBERG   (Germany)

^e LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEIN; PROTEOME; TRANSCRIPTOME; CHROMATIN;

ANIMAL CELL; ARTICLE; AXONEME; CHROMATIN; CONTROLLED STUDY; DNA REPLICATION; DRUG TARGETING; ENERGY METABOLISM; FEMALE; FERTILIZATION; GAMETE; GAMETOCYTE; GENE EXPRESSION; LIPID METABOLISM; MALE; NONHUMAN; OOCYST; PLASMODIUM FALCIPARUM; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN METABOLISM; PROTEOMICS; RNA TRANSLATION; SPOROZOITE; TRANSCRIPTOMICS; ZYGOTE; GAMETOGENESIS; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; HUMAN; MALARIA FALCIPARUM; METABOLISM; PARASITOLOGY; PATHOGENICITY; PROTEIN SYNTHESIS; SEXUAL DEVELOPMENT;

CHROMATIN; DNA REPLICATION; FEMALE; GAMETOGENESIS; GENE EXPRESSION REGULATION; HUMANS; MALARIA, FALCIPARUM; MALE; METABOLIC NETWORKS AND PATHWAYS; PLASMODIUM FALCIPARUM; PROTEIN BIOSYNTHESIS; PROTEOME; SEX CHARACTERISTICS; TRANSCRIPTOME;

EID: 84982812956     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkw536     Document Type: Article

References (73)

1. Baker, D.A. (2010) Malaria gametocytogenesis. Mol. Biochem. Parasitol., 172, 57-65.
2. 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.
3. Kooij, T.W. and Matuschewski, K. (2007) Triggers and tricks of Plasmodium sexual development. Curr. Opin. Microbiol., 10, 547-553.
4. Kuehn, A. and Pradel, G. (2010) The coming-out of malaria gametocytes. J. Biomed. Biotechnol., 976827.
5. Stone, W., Goncalves, B.P., Bousema, T. and Drakeley, C. (2015) Assessing the infectious reservoir of falciparum malaria: past and future. Trends Parasitol., 31, 287-296.
6. Hawking, F., Wilson, M.E. and Gammage, K. (1971) Evidence for cyclic development and short-lived maturity in the gametocytes of Plasmodium falciparum. Trans. R. Soc. Trop. Med. Hyg., 65, 549-559.
7. Rogers, N.J., Hall, B.S., Obiero, J., Targett, G.A. and Sutherland, C.J. (2000) A model for sequestration of the transmission stages of Plasmodium falciparum: adhesion of gametocyte-infected erythrocytes to human bone marrow cells. Infect. Immun., 68, 3455-3462.
8. Dixon, M.W., Dearnley, M.K., Hanssen, E., Gilberger, T. and Tilley, L. (2012) Shape-shifting gametocytes: how and why does P. falciparum go banana-shaped? Trends Parasitol., 28, 471-478.
9. 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.
10. 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.
11. Mair, G.R., Lasonder, E., Garver, L.S., Franke-Fayard, B.M., Carret, C.K., Wiegant, J.C., Dirks, R.W., Dimopoulos, G., Janse, C.J. and Waters, A.P. (2010) Universal features of post-transcriptional gene regulation are critical for Plasmodium zygote development. PLoS Pathog., 6, e1000767.
12. Guerreiro, A., Deligianni, E., Santos, J.M., Silva, P.A., Louis, C., Pain, A., Janse, C.J., Franke-Fayard, B., Carret, C.K., Siden-Kiamos, I. et al. (2014) Genome-wide RIP-Chip analysis of translational repressor-bound mRNAs in the Plasmodium gametocyte. Genome Biol., 15, 493-508.
13. Dixon, M.W., Thompson, J., Gardiner, D.L. and Trenholme, K.R. (2008) Sex in Plasmodium: a sign of commitment. Trends Parasitol., 24, 168-175.
14. Saeed, S., Carter, V., Tremp, A.Z. and Dessens, J.T. (2013) Translational repression controls temporal expression of the Plasmodium berghei LCCL protein complex. Mol. Biochem. Parasitol., 189, 38-42.
15. Scholz, S.M., Simon, N., Lavazec, C., Dude, M.A., Templeton, T.J. and Pradel, G. (2008) PfCCp proteins of Plasmodium falciparum: gametocyte-specific expression and role in complement-mediated inhibition of exflagellation. Int. J. Parasitol., 38, 327-340.
16. Miao, J., Fan, Q., Parker, D., Li, X., Li, J. and Cui, L. (2013) Puf mediates translation repression of transmission-blocking vaccine candidates in malaria parasites. PLoS Pathog., 9, e1003268.
17. Miao, J., Li, J., Fan, Q., Li, X., Li, X. and Cui, L. (2010) The Puf-family RNA-binding protein PfPuf2 regulates sexual development and sex differentiation in the malaria parasite Plasmodium falciparum. J. Cell Sci., 123, 1039-1049.
18. Ifediba, T. and Vanderberg, J.P. (1981) Complete in vitro maturation of Plasmodium falciparum gametocytes. Nature, 294, 364-366.
19. Ponnudurai, T., Lensen, A.H., Leeuwenberg, A.D. and Meuwissen, J.H. (1982) Cultivation of fertile Plasmodium falciparum gametocytes in semi-automated systems. 1. Static cultures. Trans. R. Soc. Trop.Med. Hyg., 76, 812-818.
20. Ponnudurai, T., Lensen, A.H., Meis, J.F. and Meuwissen, J.H. (1986) Synchronization of Plasmodium falciparum gametocytes using an automated suspension culture system. Parasitology, 93, 263-274.
21. 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. et al. (2008) Gene disruption of Plasmodium falciparum p52 results in attenuation of malaria liver stage development in cultured primary human hepatocytes. PLoS One, 3, e3549.
22. Ponnudurai, T., Lensen, A.H., Van Gemert, G.J., Bensink, M.P., Bolmer, M. and Meuwissen, J.H. (1989) Infectivity of cultured Plasmodium falciparum gametocytes to mosquitoes. Parasitology, 98, 165-173.
23. 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.
24. Trang, D.T., Huy, N.T., Kariu, T., Tajima, K. and Kamei, K. (2004) One-step concentration of malarial parasite-infected red blood cells and removal of contaminating white blood cells. Malar. J., 3, 7-13.
25. Kensche, P.R., Hoeijmakers, W.A., Toenhake, C.G., Bras, M., Chappell, L., Berriman, M. and Bartfai, R. (2015) The nucleosome landscape of Plasmodium falciparum reveals chromatin architecture and dynamics of regulatory sequences. Nucleic Acids Res., 44, 2110-2124.
26. Hoeijmakers, W.A., Bartfai, R. and Stunnenberg, H.G. (2013) Transcriptome analysis using RNA-Seq. Methods Mol. Biol., 923, 221-239.
27. Lasonder, E., Ishihama, Y., Andersen, J.S., Vermunt, A.M., Pain, A., Sauerwein, R.W., Eling, W.M., Hall, N., Waters, A.P., Stunnenberg, H.G. et al. (2002) Analysis of the Plasmodium falciparum proteome by high-accuracy mass spectrometry. Nature, 419, 537-542.
28. 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.
29. Rappsilber, J., Ishihama, Y. and Mann, M. (2003) Stop and go extraction tips for matrix-assisted laser desorption/ionization, nanoelectrospray, and LC/MS sample pretreatment in proteomics. Anal. Chem., 75, 663-670.
30. Cox, J., Neuhauser, N., Michalski, A., Scheltema, R.A., Olsen, J.V. and Mann, M. (2011) Andromeda: a peptide search engine integrated into the MaxQuant environment. J. Proteome Res., 10, 1794-1805.
31. Cox, J. and Mann, M. (2008) MaxQuant enables high peptide identification rates, individualized p.p.b.-range mass accuracies and proteome-wide protein quantification. Nat. Biotechnol., 26, 1367-1372.
32. Subramanian, A., Tamayo, P., Mootha, V.K., Mukherjee, S., Ebert, B.L., Gillette, M.A., Paulovich, A., Pomeroy, S.L., Golub, T.R., Lander, E.S. et al. (2005) Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. Proc. Natl. Acad. Sci. U.S.A., 102, 15545-15550.
33. Bauer, S., Grossmann, S., Vingron, M. and Robinson, P.N. (2008) Ontologizer 2.0-a multifunctional tool for GO term enrichment analysis and data exploration. Bioinformatics, 24, 1650-1651.
34. Iwanaga, S., Kato, T., Kaneko, I. and Yuda, M. (2012) Centromere plasmid: a new genetic tool for the study of Plasmodium falciparum. PLoS One, 7, e33326.
35. Bartfai, R., Hoeijmakers, W.A., Salcedo-Amaya, A.M., Smits, A.H., Janssen-Megens, E., Kaan, A., Treeck, M., Gilberger, T.W., Francoijs, K.J. and Stunnenberg, H.G. (2010) H2A.Z demarcates intergenic regions of the plasmodium falciparum epigenome that are dynamically marked by H3K9ac and H3K4me3. PLoS Pathog., 6, e1001223.
36. Otto, T.D., Wilinski, D., Assefa, S., Keane, T.M., Sarry, L.R., Bohme, U., Lemieux, J., Barrell, B., Pain, A., Berriman, M. et al. (2010) New insights into the blood-stage transcriptome of Plasmodium falciparum using RNA-Seq. Mol. Microbiol., 76, 12-24.
37. Kafsack, B.F., Rovira-Graells, N., Clark, T.G., Bancells, C., Crowley, V.M., Campino, S.G., Williams, A.E., Drought, L.G., Kwiatkowski, D.P., Baker, D.A. et al. (2014) A transcriptional switch underlies commitment to sexual development in malaria parasites. Nature, 507, 248-252.
38. Cox, J., Hein, M.Y., Luber, C.A., Paron, I., Nagaraj, N. and Mann, M. (2014) MaxLFQ allows accurate proteome-wide label-free quantification by delayed normalization and maximal peptide ratio extraction. Mol. Cell. Proteomics, 3, 2513-2526.
39. Eberl, H.C., Spruijt, C.G., Kelstrup, C.D., Vermeulen, M. and Mann, M. (2013) A map of general and specialized chromatin readers in mouse tissues generated by label-free interaction proteomics. Mol. Cell, 49, 368-378.
40. Hubner, N.C., Bird, A.W., Cox, J., Splettstoesser, B., Bandilla, P., Poser, I., Hyman, A. and Mann, M. (2010) Quantitative proteomics combined with BAC TransgeneOmics reveals in vivo protein interactions. J. Cell Biol., 189, 739-754.
41. Weisser, H., Nahnsen, S., Grossmann, J., Nilse, L., Quandt, A., Brauer, H., Sturm, M., Kenar, E., Kohlbacher, O., Aebersold, R. et al. (2013) An automated pipeline for high-throughput label-free quantitative proteomics. J. Proteome Res., 12, 1628-1644.
42. Deligianni, E., Morgan, R.N., Bertuccini, L., Kooij, T.W., Laforge, A., Nahar, C., Poulakakis, N., Schuler, H., Louis, C., Matuschewski, K. et al. (2011) Critical role for a stage-specific actin in male exflagellation of the malaria parasite. Cell. Microbiol., 13, 1714-1730.
43. Deligianni, E., Morgan, R.N., Bertuccini, L., Wirth, C.C., Silmon de Monerri, N.C., Spanos, L., Blackman, M.J., Louis, C., Pradel, G. and Siden-Kiamos, I. (2013) A perforin-like protein mediates disruption of the erythrocyte membrane during egress of Plasmodium berghei male gametocytes. Cell. Microbiol., 15, 1438-1455.
44. Dorin-Semblat, D., Schmitt, S., Semblat, J.P., Sicard, A., Reininger, L., Goldring, D., Patterson, S., Quashie, N., Chakrabarti, D., Meijer, L. et al. (2011) Plasmodium falciparum NIMA-related kinase Pfnek-1: sex specificity and assessment of essentiality for the erythrocytic asexual cycle. Microbiology, 157, 2785-2794.
45. Eksi, S., Suri, A. and Williamson, K.C. (2008) Sex-and stage-specific reporter gene expression in Plasmodium falciparum. Mol. Biochem. Parasitol., 160, 148-151.
46. Eksi, S. and Williamson, K.C. (2002) Male-specific expression of the paralog of malaria transmission-blocking target antigen Pfs230, PfB0400w. Mol. Biochem. Parasitol., 122, 127-130.
47. Hirai, M., Arai, M., Mori, T., Miyagishima, S.Y., Kawai, S., Kita, K., Kuroiwa, T., Terenius, O. and Matsuoka, H. (2008) Male fertility of malaria parasites is determined by GCS1, a plant-type reproduction factor. Curr. Biol., 18, 607-613.
48. Laurentino, E.C., Taylor, S., Mair, G.R., Lasonder, E., Bartfai, R., Stunnenberg, H.G., Kroeze, H., Ramesar, J., Franke-Fayard, B., Khan, S.M. et al. (2011) Experimentally controlled downregulation of the histone chaperone FACT in Plasmodium berghei reveals that it is critical to male gamete fertility. Cell. Microbiol., 13, 1956-1974.
49. Rangarajan, R., Bei, A.K., Jethwaney, D., Maldonado, P., Dorin, D., Sultan, A.A. and Doerig, C. (2005) A mitogen-activated protein kinase regulates male gametogenesis and transmission of the malaria parasite Plasmodium berghei. EMBO Rep., 6, 464-469.
50. Tewari, R., Straschil, U., Bateman, A., Bohme, U., Cherevach, I., Gong, P., Pain, A. and Billker, O. (2010) The systematic functional analysis of Plasmodium protein kinases identifies essential regulators of mosquito transmission. Cell Host Microbe, 8, 377-387.
51. de Koning-Ward, T.F., Olivieri, A., Bertuccini, L., Hood, A., Silvestrini, F., Charvalias, K., Berzosa Diaz, P., Camarda, G., McElwain, T.F., Papenfuss, T. et al. (2008) The role of osmiophilic bodies and Pfg377 expression in female gametocyte emergence and mosquito infectivity in the human malaria parasite Plasmodium falciparum. Mol. Microbiol., 67, 278-290.
52. 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.
53. Tran, P.N., Brown, S.H., Mitchell, T.W., Matuschewski, K., McMillan, P.J., Kirk, K., Dixon, M.W. and Maier, A.G. (2014) A female gametocyte-specific ABC transporter plays a role in lipid metabolism in the malaria parasite. Nat. Commun., 5, 4773-4785.
54. van Schaijk, B.C., van Dijk, M.R., van de Vegte-Bolmer, M., 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.
55. Tao, D., Ubaida-Mohien, C., Mathias, D.K., King, J.G., Pastrana-Mena, R., Tripathi, A., Goldowitz, I., Graham, D.R., Moss, E., Marti, M. et al. (2014) Sex-partitioning of the Plasmodium falciparum stage V gametocyte proteome provides insight into falciparum-specific cell biology. Mol. Cell. Proteomics, 13, 2705-2724.
56. Ishihama, Y., Oda, Y., Tabata, T., Sato, T., Nagasu, T., Rappsilber, J. and Mann, M. (2005) Exponentially modified protein abundance index (emPAI) for estimation of absolute protein amount in proteomics by the number of sequenced peptides per protein. Mol. Cell. Proteomics, 4, 1265-1272.
57. Reddy, B.P., Shrestha, S., Hart, K.J., Liang, X., Kemirembe, K., Cui, L. and Lindner, S.E. (2015) A bioinformatic survey of RNA-binding proteins in Plasmodium. BMC Genomics, 16, 890-915.
58. Bell, S.D., Botting, C.H., Wardleworth, B.N., Jackson, S.P. and White, M.F. (2002) The interaction of Alba, a conserved archaeal chromatin protein, with Sir2 and its regulation by acetylation. Science, 296, 148-151.
59. Kangwanrangsan, N., Tachibana, M., Jenwithisuk, R., Tsuboi, T., Riengrojpitak, S., Torii, M. and Ishino, T. (2013) A member of the CPW-WPC protein family is expressed in and localized to the surface of developing ookinetes. Malar. J., 12, 129-138.
60. Braks, J.A., Mair, G.R., Franke-Fayard, B., Janse, C.J. and Waters, A.P. (2008) A conserved U-rich RNA region implicated in regulation of translation in Plasmodium female gametocytes. Nucleic Acids Res., 36, 1176-1186.
61. 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. et al. (2005) A comprehensive survey of the Plasmodium life cycle by genomic, transcriptomic, and proteomic analyses. Science, 307, 82-86.
62. Cui, L., Lindner, S. and Miao, J. (2015) Translational regulation during stage transitions in malaria parasites. Ann. N.Y. Acad. Sci., 1342, 1-9.
63. Gomes-Santos, C.S., Braks, J., Prudencio, M., Carret, C., Gomes, A.R., Pain, A., Feltwell, T., Khan, S., Waters, A., Janse, C. et al. (2011) Transition of Plasmodium sporozoites into liver stage-like forms is regulated by the RNA binding protein Pumilio. PLoS Pathog., 7, e1002046.
64. van Schaijk, B.C., Kumar, T.R., Vos, M.W., Richman, A., van Gemert, G.J., Li, T., Eappen, A.G., Williamson, K.C., Morahan, B.J., Fishbaugher, M. et al. (2014) Type II fatty acid biosynthesis is essential for Plasmodium falciparum sporozoite development in the midgut of Anopheles mosquitoes. Eukaryot Cell, 13, 550-559.
65. Santos, J.M., Kehrer, J., Franke-Fayard, B., Frischknecht, F., Janse, C.J. and Mair, G.R. (2015) The Plasmodium palmitoyl-S-acyl-transferase DHHC2 is essential for ookinete morphogenesis and malaria transmission. Sci. Rep., 5, 16034-16043.
66. Angrisano, F., Tan, Y.H., Sturm, A., McFadden, G.I. and Baum, J. (2012) Malaria parasite colonisation of the mosquito midgut-placing the Plasmodium ookinete centre stage. Int. J. Parasitol., 42, 519-527.
67. Lal, K., Prieto, J.H., Bromley, E., Sanderson, S.J., Yates, J.R. 3rd, Wastling, J.M., Tomley, F.M. and Sinden, R.E. (2009) Characterisation of Plasmodium invasive organelles; an ookinete microneme proteome. Proteomics, 9, 1142-1151.
68. Talman, A.M., Prieto, J.H., Marques, S., Ubaida-Mohien, C., Lawniczak, M., Wass, M.N., Xu, T., Frank, R., Ecker, A., Stanway, R.S. et al. (2014) Proteomic analysis of the Plasmodium male gamete reveals the key role for glycolysis in flagellar motility. Malar. J., 13, 315-326.
69. Pradel, G., Hayton, K., Aravind, L., Iyer, L.M., Abrahamsen, M.S., Bonawitz, A., Mejia, C. and Templeton, T.J. (2004) A multidomain adhesion protein family expressed in Plasmodium falciparum is essential for transmission to the mosquito. J. Exp. Med., 199, 1533-1544.
70. 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 multi-protein complexes in the malaria parasite Plasmodium falciparum. J. Biol. Chem., 284, 14537-14546.
71. Patra, K.P., Johnson, J.R., Cantin, G.T., Yates, J.R. 3rd and Vinetz, J.M. (2008) Proteomic analysis of zygote and ookinete stages of the avian malaria parasite Plasmodium gallinaceum delineates the homologous proteomes of the lethal human malaria parasite Plasmodium falciparum. Proteomics, 8, 2492-2499.
72. Lasonder, E., Janse, C.J., van Gemert, G.J., Mair, G.R., Vermunt, A.M., Douradinha, B.G., van Noort, V., Huynen, M.A., Luty, A.J., Kroeze, H. et al. (2008) Proteomic profiling of Plasmodium sporozoite maturation identifies new proteins essential for parasite development and infectivity. PLoS Pathog., 4, e1000195.
73. Lindner, S.E., Swearingen, K.E., Harupa, A., Vaughan, A.M., Sinnis, P., Moritz, R.L. and Kappe, S.H. (2013) Total and putative surface proteomics of malaria parasite salivary gland sporozoites. Mol. Cell. Proteomics, 12, 1127-1143.