Transcriptional responses of Plasmodium falciparum to α- difluoromethylornithine-induced polyamine depletion

Biological Chemistry

Volumn 389, Issue 2, 2008, Pages 111-125

  Clark, Katherine ^a   Dhoogra, Minishca ^a   Louw, Abraham I ^a,b   Birkholtz, Lyn Marié ^a,b  

^a UNIVERSITY OF PRETORIA   (South Africa)

^b African Centre for Gene Technologies   (South Africa)

Author keywords

Malaria; Microarray; Suppression subtractive hybridisation; Transcriptome

Indexed keywords

EFLORNITHINE; POLYAMINE;

ARTICLE; CONTROLLED STUDY; DNA MICROARRAY; GENE EXPRESSION; GENE SEQUENCE; GENETIC TRANSCRIPTION; HYBRIDIZATION; NONHUMAN; PLASMODIUM FALCIPARUM; PRIORITY JOURNAL;

ANIMALS; EFLORNITHINE; FEEDBACK, BIOCHEMICAL; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; HUMANS; ORNITHINE DECARBOXYLASE; PLASMODIUM FALCIPARUM; POLYAMINES; TRANSCRIPTION, GENETIC;

PLASMODIUM FALCIPARUM;

EID: 38649087079     PISSN: 14316730     EISSN: 14374315     Source Type: Journal    
DOI: 10.1515/BC.2008.014     Document Type: Article

References (57)

1. Ackermann, J.M., Pegg, A.E., and McCloskey, D.E. (2003). Drugs affecting the cell cycle via actions on the polyamine metabolic pathway. Prog. Cell Cycle Res. 5, 461-468.
2. 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 malaria parasite, Plasmodium falciparum. Biochem. J. 222, 815-819.
3. Assaraf, Y.G., Abu-Elheiga, L., Spira, D.T., Desser, H., and Bachrach, U. (1987a). Effect of polyamine depletion on macromolecular synthesis of the malarial parasite, Plasmodium falciparum, cultured in human erythrocytes. Biochem. J. 242, 221-226.
4. Assaraf, Y.G., Golenser, J., Spira, D.T., Messer, G., and Bachrach, U. (1987b). Cytostatic effect of DL-α-difluoromethylornithine against Plasmodium falciparum and its reversal by diamines and spermidine. Parasitol. Res. 73, 313-318.
5. Bell, D.R., Jorgensen, P., Christophel, E.M., and Palmer, K.L. (2005). Malaria risk: estimation of the malaria burden. Nature 437, E3-4.
6. Birkholtz, L., Bastien, O., Wells, G., Grando, D., Joubert, F., Kasam, V., Zimmerman, M., Ortet, P., Jacq, N., Saidani, N., et al. (2006). Integration and mining of malaria molecular, functional and pharmacological data: how far are we from a chemogenomic knowledge space? Malaria J. 5, 110.
7. 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.
8. Bitonti, A.J., Dumont, J.A., Bush, T.L., Edwards, M.L., Stemerick, D.M., McCann, P.P., and Sjoerdsma, A. (1989). Bis(benzyl)polyamine analogs inhibit the growth of chloroquine-resistant human malaria parasites (Plasmodium falciparum) in vitro and in combination with a-difluoromethylornithine cure murine malaria. Proc. Natl. Acad. Sci. USA 86, 651-655.
9. Bozdech, Z., Llinás, M., Pulliam, B.L., Wong, E.D., Zhu, J., and DeRisi, J.L. (2003). The transcriptome of the intraerythrocytic developmental cycle of Plasmodium falciparum. PLoS Biol. 1, E5.
10. Childs, A.C., Metha, D.J., and Gerner, E.W. (2003). Polyamine-dependent gene expression. Cell Mol. Life Sci. 60, 1394-1406.
11. Cohen, S.S. (1998). A Guide to the Polyamines (Oxford, UK: Oxford University Press).
12. Cowman, A.F. and Crabb, B.S. (2006). Invasion of red blood cells by malaria parasites. Cell 124, 755-766.
13. Das Gupta, R., Krause-Ilhe, T., Bergmann, B., Müller, I.B., Khomutov, A.R., Müller, S., Walter, R.D., and Luersen, K. (2005). 3-Aminooxy-1-aminopropane and derivatives have an antiproliferative effect on cultured Plasmodium falciparum by decreasing intracellular polyamine concentrations. Antimicrob. Agents Chemother. 49, 2857-2864.
14. DePristo, M.A., Zilversmit, M.M., and Hartl, D.L. (2006). On the abundance, amino acid composition, and evolutionary dynamics of low-complexity regions in proteins. Gene 378, 19-30.
15. Desai, S., Hill, J., Trelogan, S., Diatchenko, L., and Siebert, P.D. (2000). Identification of differentially expressed genes by suppression subtractive hybridisation. In: Functional Genomics: A Practical Approach, S.P. Hunt and R.J. Livesey, eds. (Oxford, UK: Oxford University Press), pp. 81-112.
16. Dessens, J.T., Margos, G., Rodriguez, M.C., and Sinden, R.E. (2000). Identification of differentially regulated genes of Plasmodium falciparum by suppression subtractive hybridisation. Parasitol. Today 16, 354-356.
17. Diatchenko, L., Lau, Y.F., Campbell, A.P., Chenchik, A., Moqadam, F., Huang, B., Lukyanov, S., Lukyanov, K., Gurskaya, N., Sverdlov, E.D., et al. (1996). Suppression subtractive hybridization: a method for generating differentially regulated or tissue-specific cDNA probes and libraries. Proc. Natl. Acad. Sci. USA 93, 6025-6030.
18. 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., et al. (2002). A proteomic view of the Plasmodium falciparum life cycle. Nature 419, 520-526.
19. Florent, I., Charneau, S., and Grellier, P. (2004). Plasmodium falciparum genes differentially expressed during merozoite morphogenesis. Mol. Biochem. Parasitol. 135, 143-148.
20. Gafan, C., Wilson, J., Berger, L.C., and Berger, B.J. (2001). Characterisation of the ornithine aminotransferase from Plasmodium falciparum. Mol. Biochem. Parasitol. 118, 1-10.
21. Gardner, M.J., Hall, N., Fung, E., White, O., Berriman, M., Hyman, R.W., Carlton, J.M., Pain, A., Nelson, K.E., Bowman, S., et al. (2002). Genome sequence of the human malaria parasite Plasmodium falciparum. Nature 419, 498-511.
22. Gentleman, R.C., Carey, V.J., Bates, D.M., Bolstad, B., Dettling, M., Dudoit, S., Ellis, B., Gautier, L., Ge, Y., Gentry, J., et al. (2004). Bioconductor: open software development for computational biology and bioinformatics. Genome Biol. 5, R80.
23. Ghosh, A., Srinivasan, P., Abraham, E.G., Fujioka, H., and Jacobs-Lorena, M. (2003). Molecular strategies to study Plasmodium-mosquito interactions. Trends Parasitol. 19, 94-101.
24. Gunasekera, A.M., Patankar, S., Schug, J., Eisen, G., and Wirth, D.F. (2003). Drug-induced alterations in gene expression of the asexual blood forms of Plasmodium falciparum. Mol. Microbiol. 50, 1229-1239.
25. Gunasekera, A.M., Myrick, A., Le Roch, K., Winzeler, E., and Wirth, D.F. (2007a). Plasmodium falciparum: genome wide perturbations in transcript profiles among mixed stage cultures after chloroquine treatment. Exp. Parasitol. 117, 87-92.
26. Gunasekera, A.M., Myrick, A., Militello, K.T., Sims, J.S., Dong, C.K., Gierahn, T., Le Roch, K., Winzeler, E., and Wirth, D.F. (2007b). Regulatory motifs uncovered among gene expression clusters in Plasmodium falciparum. Mol. Biochem. Parasitol. 153, 19-30.
27. Heby, O., Roberts, S.C., and Ullman, B. (2003). Polyamine biosynthetic enzymes as drug targets in parasitic protozoa. Biochem. Soc. Trans. 31, 415-419.
28. Janne, J., Alhonen, L., Pietila, M., and Keinanen, T.A. (2004). Genetic approaches to the cellular functions of polyamines in mammals. Eur. J. Biochem. 271, 877-894.
29. Kaiser, A., Gottwald, A., Wiersch, C., Lindenthal, B., Maier, W., and Seitz, H.M. (2001). Effect of drugs inhibiting spermidine biosynthesis and metabolism on the in vitro development of Plasmodium falciparum. Parasitol. Res. 87, 963-972.
30. Kaiser, A., Gottwald, A., Maier, W., and Seitz, H.M. (2003). Targeting enzymes involved in spermidine metabolism of parasitic protozoa - a possible new strategy for anti-parasitic treatment. Parasitol. Res. 91, 508-516.
31. Kaiser, A., Ulmer, D., Goebel, T., Holzgrabe, U., Saeftel, M., and Hoerauf, A. (2006). Inhibition of hypusine biosynthesis in Plasmodium: a possible, new strategy in prevention and therapy of malaria. Mini Rev. Med. Chem. 6, 1231-1241.
32. Kawazu, S., Ikenoue, N., Takemae, H., Komaki-Yasuda, K., and Kano, S. (2005). Roles of 1-cys peroxiredoxin in haem detoxification in the human malaria parasite Plasmodium falciparum. FEBS J. 272, 1784-1791.
33. Klemba, M., Gluzman, I., and Goldberg, D.E. (2004). A Plasmodium falciparum dipeptidyl aminopeptidase I participates in vacuolar hemoglobin degradation. J. Biol. Chem. 279, 43000-43007.
34. Lambros, C. and Vanderberg, J.P. (1979). Synchronization of Plasmodium falciparum erythrocytic stages in culture. J. Parasitol. 65, 418-420.
35. Lanzer, M., Wickert, H., Krohne, G., Vincensini, L., and Braun Breton, C. (2006). Maurer's clefts: a novel multi-functional organelle in the cytoplasm of Plasmodium falciparum-infected erythrocytes. Int. J. Parasitol. 36, 23-36.
36. Le Roch, K.G., Johnson, J.R., Florens, L., Zhou, Y., Santrosyan, A., Grainger, M., Yan, F., Williamson, K.C., Holder, A.A., Carucci, D.J., et al. (2004). Global analysis of transcript and protein levels across the Plasmodium falciparum life cycle. Genome Res. 14, 2308-2318.
37. Loikkannen, I. (2005). Polyamine homeostasis: cellular responses to perturbation of polyamine biosynthetic enzymes. Ph.D. thesis (Oulu, Finland: University of Oulu).
38. Madeira, L., DeMarco, R., Gazarini, M.L., Verjovski-Almeida, S., and Garcia, C.R.S. (2003). Human malaria parasites display a receptor for activated C kinase ortholog. Biochem. Biophys. Res. Commun. 306, 995-1001.
39. Martin, R.E., Henry, R.I., Abbey, J.L., Clements, J.D., and Kirk, K. (2005). The 'permeome' of the malaria parasite: an overview of the membrane transport proteins of Plasmodium falciparum. Genome Biol. 6, R26.
40. Marton, L.J. and Pegg, A.E. (1995). Polyamines as targets for therapeutic intervention. Annu. Rev. Pharmacol. Toxicol. 35, 55-91.
41. McCann, P.P. and Pegg, A.E. (1992). Ornithine decarboxylase as an enzyme target for therapy. Pharmacol. Ther. 54, 195-215.
42. Moritz, E., Seindensticker, S., Gottwald, A., Maier, W., Hoerauf, A., Njuguna, F.T., and Kaiser, A. (2004). The efficacy of inhibitors involved in spermidine metabolism in Plasmodium falciparum, Anopheles stephensi and Trypanosoma evansi. Parasitol. Res. 94, 37-48.
43. Müller, S., Coombs, G.H., and Walter, R.D. (2001). Targeting polyamines of parasitic protozoa in chemotherapy. Trends Parasitol. 17, 242-249.
44. Shi, W., Ting, L., Kicska, G.A., Lewandowicz, A., Tyler, P.C., Evans, G.B., Furneaux, R.H., Kim, K., Almo, S.C., and Schramm, V.L. (2004). Plasmodium falciparum purine nucleoside phosphorylase. J. Biol. Chem. 279, 18103-18106.
45. Spielmann, T. and Beck, H.P. (2000). Analysis of stage-specific transcription in Plasmodium falciparum reveals a set of genes exclusively transcribed in ring stage parasites. Mol. Biochem. Parasitol. 111, 453-458.
46. Sufrin, J.R., Meshnick, S.R., Spiess, A.J., Garofalo-Hannan, J., Pan, X., and Bacchi, C.J. (1995). Methionine recycling pathways and antimalarial drug design. Antimicrob. Agents Chemother. 39, 2511-2515.
47. Teti, D., Visalli, M., and McNair, H. (2002). Analysis of polyamines as markers of (patho)physiological conditions. J. Chromatogr. 781, 107-149.
48. Ting, L., Shi, W., Lewandowicz, A., Singh, V., Mwakingwe, A., Birck, M., Ringia, E.A.T., Bench, G., Madrid, D.C., Tyler, P.C., et al. (2005). Targeting a novel Plasmodium falciparum purine recycling pathway with specific immunicillins. J. Biol. Chem. 280, 9547-9554.
49. Trager, W. and Jensen, J.B. (1976). Human malaria parasites in continuous culture. Science 193, 673-675.
50. van den Berg, N., Crampton, B.G., Hein, I., Birch, P.R.J., and Berger, D.K. (2004). High-throughput screening of suppression subtractive hybridization cDNA libraries using DNA microarray analysis. BioTechniques 37, 818-824.
51. Vincensini, L., Richert, S., Blisnick, T., Van Dorsselaer, A., Leize-Wagner, E., Rabilloud, T., and Braun Breton, C. (2005). Proteomic analysis identifies novel proteins of the Maurer's clefts, a secretory compartment delivering Plasmodium falciparum proteins to the surface of its host cell. Mol. Cell. Proteomics 4, 582-593.
52. Wallace, H.M., Fraser, A.V., and Hughes, A. (2003). A perspective on polyamine metabolism. Biochem. J. 376, 1-14.
53. Wang, C.C. (1995). Molecular mechanisms and therapeutic approaches to the treatment of African trypanosomiasis. Annu. Rev. Pharmacol. Toxicol. 35, 93-127.
54. Ward, P., Equinet, L., Packer, J., and Doerig, C. (2004). Protein kinases of the human malaria parasite Plasmodium falciparum: the kinome of a divergent eukaryote. BMC Genomics 5, 79.
55. Wettenhall, J.M. and Smyth, G.K. (2004). limmaGUI: a graphical user interface for linear modeling of microarray data. Bioinformatics 20, 3705-3706.
56. Yoshida, M., Kashiwagi, K., Shigemasa, A., Taniguchi, S., Yamamoto, K., Makinoshima, M., Ishihama, A., and Igarashi, K. (2004). A unifying model for the role of polyamines in bacterial cell growth, the polyamine modulon. J. Biol. Chem. 44, 46008-46013.
57. Young, J.A. and Winzeler, E.A. (2005). Using expression information to discover new drug and vaccine targets in the malaria parasite Plasmodium falciparum. Pharmacogenomics 6, 1-26.