Plasmodium AdoMetDC/ODC bifunctional enzyme is essential for male sexual stage development and mosquito transmission

Biology Open

Volumn 5, Issue 8, 2016, Pages 1022-1029

  Hart, Robert J ^a   Ghaffar, Atif ^a   Abdalal, Shaymaa ^a   Perrin, Benjamin ^a   Aly, Ahmed S I ^a  

^a TULANE UNIVERSITY   (United States)

Author keywords

Anopheles; Malaria; Plasmodium; Polyamines; S adenosyl methionine decarboxylase ornithine decarboxylase; Sexual stages

Indexed keywords

ADENOSYLMETHIONINE DECARBOXYLASE; ORNITHINE DECARBOXYLASE; POLYAMINE; PUTRESCINE; SPERMIDINE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANOPHELES; ARTICLE; CONTROLLED STUDY; DEVELOPMENTAL STAGE; ENZYME ACTIVITY; ENZYME SYNTHESIS; FEMALE; GAMETE; GAMETOCYTE; GAMETOGENESIS; GENE DELETION; HOMEOSTASIS; MALE; MOSQUITO; MOUSE; NONHUMAN; OOCYST; PARASITE TRANSMISSION; PHENOTYPE; PLASMODIUM (LIFE CYCLE STAGE); PLASMODIUM YOELII; SEXUAL DEVELOPMENT; SPOROZOITE;

EID: 84986000554     PISSN: None     EISSN: 20466390     Source Type: Journal    
DOI: 10.1242/bio.016352     Document Type: Article

References (33)

1. 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. et al. (2011). A research agenda to underpin malaria eradication. PLoS Med. 8, e1000406.
2. Aly, A. S. I., Vaughan, A. M. and Kappe, S. H. I. (2009). Malaria parasite development in the mosquito and infection of the mammalian host. Annu. Rev. Microbiol. 63, 195-221.
3. Aly, A. S. I., Downie, M. J., Mamoun, C. B. and Kappe, S. H. I. (2010). Subpatent infection with nucleoside transporter 1-deficient Plasmodium blood stage parasites confers sterile protection against lethal malaria in mice. Cell. Microbiol. 12, 930-938.
4. Assaraf, Y. G., Golenser, J., Spira, D. T. and Bachrach, U. (1984). Polyamine levels and the activity of their biosynthetic enzymes in human erythrocytes infected with the malarial parasite, Plasmodium falciparum. Biochem. J. 222, 815-819.
5. Birkholtz, L.-M., Williams, M., Niemand, J., Louw, A. I., Persson, L. and Heby, O. (2011). Polyamine homoeostasis as a drug target in pathogenic protozoa: peculiarities and possibilities. Biochem. J. 438, 229-244.
6. Bitonti, A. J., McCann, P. P. and Sjoerdsma, A. (1987). Plasmodium falciparum and Plasmodium berghei: effects of ornithine decarboxylase inhibitors on erythrocytic schizogony. Exp. Parasitol. 64, 237-243.
7. Burger, P. B., Williams, M., Sprenger, J., Reeksting, S. B., Botha, M., Müller, I. B., Joubert, F., Birkholtz, L.-M. and Louw, A. I. (2015). A novelinhibitorofPlasmodium falciparum spermidine synthase: a twist in the tail. Malar. J. 14,54.
8. Fairhurst, R. M. (2015). Understanding artemisinin-resistant malaria: what a difference a year makes. Curr. Opin. Infect Dis. 28, 417-425.
9. Gillet, J. M., Charlier, J., Bone?, G. and Mulamba, P. L. (1983). Plasmodium berghei: inhibition of the sporogonous cycle by alpha-difluoromethylornithine. Exp. Parasitol. 56, 190-193.
10. Hart, R. J., Lawres, L., Fritzen, E., Mamoun, C. B. and Aly, A. S. (2014). Plasmodium yoelii Vitamin B5 pantothenate transporter candidate is essential for parasite transmission to the mosquito. Sci. Rep. 4, 5665.
11. Heby, O., Roberts, S. C. and Ullman, B. (2003). Polyamine biosynthetic enzymes as drug targets in parasitic protozoa. Biochem. Soc. Trans. 31, 415-419.
12. Heby, O., Persson, L. and Rentala, M. (2007). Targeting the polyamine biosynthetic enzymes: a promising approach to therapy of African sleeping sickness, Chagas' disease, and leishmaniasis. Amino Acids 33, 359-366.
13. Hollingdale, M. R., McCann, P. P. and Sjoerdsma, A. (1985). Plasmodium berghei: inhibitors of ornithine decarboxylase block exoerythrocytic schizogony. Exp. Parasitol. 60, 111-117.
14. Janse, C. J., Franke-Fayard, B., Mair, G. R., Ramesar, J., Thiel, C., Engelmann, S., Matuschewski, K., van Gemert, G. J., Sauerwein, R. W. and Waters, A. P. (2006). High efficiency transfection of Plasmodium berghei facilitates novel selection procedures. Mol. Biochem. Parasitol. 145, 60-70.
15. Kafsack, B. F. C., 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.
16. Krause, T., Lu?ersen, K., Wrenger, C., Gilberger, T.-W., Mu?ller, S. and Walter, R. D. (2000). The ornithine decarboxylase domain of the bifunctional ornithine decarboxylase/S-adenosylmethionine decarboxylase of Plasmodium falciparum: recombinant expression and catalytic properties of two different constructs. Biochem. J. 352, 287-292.
17. Lin, J.-W., Annoura, T., Sajid, M., Chevalley-Maurel, S., Ramesar, J., Klop, O., Franke-Fayard, B. M. D., Janse, C. J. and Khan, S. M. (2011). A novel 'gene insertion/marker out' (GIMO) method for transgene expression and gene complementation in rodent malaria parasites. PLoS ONE 6, e29289.
18. Lin, J. T., Saunders, D. L. and Meshnick, S. R. (2014). The role of submicroscopic parasitemia in malaria transmission: what is the evidence? Trends Parasitol. 30, 183-190.
19. Manzoni, G., Briquet, S., Risco-Castillo, V., Gaultier, C., Topçu, S., Iva?nescu, M. L., Franetich, J.-F., Hoareau-Coudert, B., Mazier, D. and Silvie, O. (2014). A rapid and robust selection procedure for generating drug-selectable marker-free recombinant malaria parasites. Sci. Rep. 4, 4760.
20. Mu?ller, S., Da'dara, A., Lu?ersen, K., Wrenger, C., Das Gupta, R., Madhubala, R. and Walter, R. D. (2000). In the human malaria parasite Plasmodium falciparum, polyamines are synthesized by a bifunctional ornithine decarboxylase, S-adenosylmethionine decarboxylase. J. Biol. Chem. 275, 8097-8102.
21. Niemand, J., Louw, A. I., Birkholtz, L. and Kirk, K. (2012). Polyamine uptake by the intraerythrocytic malaria parasite, Plasmodium falciparum. Int. J. Parasitol. 42, 921-929.
22. Pegg, A. E. (2009). Mammalian polyamine metabolism and function. IUBMB Life 61, 880-894.
23. Ramakrishnan, C., Delves, M. J., Lal, K., Blagborough, A. M., Butcher, G., Baker, K. W. and Sinden, R. E. (2013). Laboratory maintenance of rodent malaria parasites. Methods Mol. Biol. 923, 51-72.
24. Ramya, T. N. C., Surolia, N. and Surolia, A. (2006). Polyamine synthesis and salvage pathways in the malaria parasite Plasmodium falciparum. Biochem. Biophys. Res. Commun. 348, 579-584.
25. Reguera, R. M., Tekwani, B. L. and Balan?a-Fouce, R. (2005). Polyamine transport in parasites: a potential target for new antiparasitic drug development. Comp. Biochem. Physiol. C Toxicol. Pharmacol. 140, 151-164.
26. Rial, N. S., Meyskens, F. L. and Gerner, E. W. (2009). Polyamines as mediators of APC-dependent intestinal carcinogenesis and cancer chemoprevention. Essays Biochem. 46, 111-124.
27. Sinha, A., Hughes, K. R., Modrzynska, K. K., Otto, T. D., Pfander, C., Dickens, N. J., Religa, A. A., Bushell, E., Graham, A. L., Cameron, R. et al. (2014). A cascade of DNA-binding proteins for sexual commitment and development in Plasmodium. Nature 507, 253-257.
28. Sprenger, J., Svensson, B., Hålander, J., Carey, J., Persson, L. and Al-Karadaghi, S. (2015). Three-dimensional structures of Plasmodium falciparum spermidine synthase with bound inhibitors suggest new strategies for drug design. Acta Crystallogr. D Biol. Crystallogr. 71, 484-493.
29. St Laurent, B., Miller, B., Burton, T. A., Amaratunga, C., Men, S., Sovannaroth, S., Fay, M. P., Miotto, O., Gwadz, R. W., Anderson, J. M. et al. (2015). Artemisinin-resistant Plasmodium falciparum clinical isolates can infect diverse mosquito vectors of Southeast Asia and Africa. Nat. Commun. 6, 8614.
30. van Dijk, M. R., van Schaijk, B. C. L., Khan, S. M., van Dooren, M. W., Ramesar, J., Kaczanowski, S., van Gemert, G.-J., Kroeze, H., Stunnenberg, H. G., Eling, W. M. et al. (2010). Three members of the 6-cys protein family of Plasmodium play a role in gamete fertility. PLoS Pathog. 6, e1000853.
31. Wallace, H. M. (2009). The polyamines: past, present and future. Essays Biochem. 46, 1-10.
32. Waters, A. P. (2016). Epigenetic roulette in blood stream plasmodium: gambling on sex. PLoS Pathog. 12, e1005353.
33. Wrenger, C., Luersen, K., Krause, T., Muller, S. and Walter, R. D. (2001). The Plasmodium falciparum bifunctional ornithine decarboxylase, S-adenosyl-Lmethionine decarboxylase, enables a well balanced polyamine synthesis without domain-domain interaction. J. Biol. Chem. 276, 29651-29656.