RNA Interference-mediated silencing of ornithine decarboxylase and spermidine synthase genes in trypanosoma brucei provides insight into regulation of polyamine biosynthesis

Eukaryotic Cell

Volumn 8, Issue 5, 2009, Pages 747-755

  Xiao, Yanjing ^a   McCloskey, Diane E ^b   Phillips, Margaret A ^a  

^a UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^b PENN STATE COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSYLMETHIONINE DECARBOXYLASE; DRUG DERIVATIVE; GLUTATHIONE; ORNITHINE DECARBOXYLASE; POLYAMINE; PROTOZOAL PROTEIN; SPERMIDINE; SPERMIDINE SYNTHASE; TRYPANOTHIONE;

AFRICAN TRYPANOSOMIASIS; ANIMAL; ARTICLE; CELL LINE; ENZYMOLOGY; GENETICS; HUMAN; METABOLISM; PARASITOLOGY; RNA INTERFERENCE; TRYPANOSOMA BRUCEI;

ADENOSYLMETHIONINE DECARBOXYLASE; ANIMALS; CELL LINE; GLUTATHIONE; HUMANS; ORNITHINE DECARBOXYLASE; POLYAMINES; PROTOZOAN PROTEINS; RNA INTERFERENCE; SPERMIDINE; SPERMIDINE SYNTHASE; TRYPANOSOMA BRUCEI BRUCEI; TRYPANOSOMIASIS, AFRICAN;

TRYPANOSOMA BRUCEI;

EID: 66149158543     PISSN: 15359778     EISSN: None     Source Type: Journal    
DOI: 10.1128/EC.00047-09     Document Type: Article

References (41)

1. Ariyanayagam, M. R., S. L. Oza, M. L. S. Guther, and A. H. Fairlamb 2005. Phenotypic analysis of trypanothione synthetase knockdown in the African trypanosome. Biochem. J391:425-432.
2. Bacchi, C., H. Nathan, S. Hunter, P. McCann, and A. Sjoerdsma 1980. Polyamine metabolism: a potential therapeutic target in trypanosomes. Science 210:332-334.
3. Bacchi, C. J., R. Brun, S. L. Croft, K. Alicea, and Y. Buhler 1996. In vivo trypanocidal activities of new S-adenosylmethionine decarboxylase inhibitors. Antimicrob. Agents Chemother40:1448-1453.
4. Bacchi, C. J., J. Garofalo, D. Mockenhaupt, P. P. McCann, K. A. Diekema,A. E. Pegg, H. C. Nathan, E. A. Mullaney, L. Chunosoff, A. Sjoerdsma, and S. H. Hutner 1983. In vivo effects of alpha-DL-difluoromethylornithine on the metabolism and morphology of Trypanosoma brucei brucei. Mol. Biochem. Parasitol7:209-225.
5. Bacchi, C. J., H. C. Nathan, N. Yarlett, B. Goldberg, P. P. McCann, A. J. Bitonti, and A. Sjoerdsma 1992. Cure of murine Trypanosoma brucei rhodesienseinfections with an S-adenosylmethionine decarboxylase inhibitor. Antimicrob. Agents Chemother36:2736-2740.
6. Barrett, M. P., D. W. Boykin, R. Brun, and R. R. Tidwell 2007. Human African trypanosomiasis: pharmacological re-engagement with a neglected disease. Br. J. Pharmacol152:1155-1171.
7. Bitonti, A. J., T. L. Byers, T. L. Bush, P. J. Casara, C. J. Bacchi, A. B. Clarkson, Jr., P. P. McCann, and A. Sjoerdsma 1990. Cure of Trypanosoma brucei bruceiand Trypanosoma brucei rhodesienseinfections in mice with an irreversible inhibitor of S- adenosylmethionine decarboxylase. Antimicrob.Agents Chemother34:1485- 1490.
8. Casero, R. A., Jr., and L. J. Marton 2007. Targeting polyamine metabolism and function in cancer and other hyperproliferative diseases. Nat. Rev. Drug Discov6:373-390.
9. Childs, A. C., D. J. Mehta, and E. W. Gerner 2003. Polyamine-dependent gene expression. Cell. Mol. Life Sci60:1394-1406.
10. Coffino, P 2001. Regulation of cellular polyamines by antizyme. Nat. Rev. Mol. Cell Biol2:188-194.
11. Fairlamb, A. H., G. B. Henderson, C. J. Bacchi, and A. Cerami 1987. In vivo effects of difluoromethylornithine on trypanothione and polyamine levels in bloodstream forms of T. brucei. Mol. Biochem. Parasitol24:185-191.
12. Fries, D. S., and A. H. Fairlamb 2003. Antiprotozoal agents, p. 1033-1087. InD. Abraham (ed.), Burger's medicinal chemistry and drug discovery, 6th ed., vol. 5. John Wiley & Sons, Inc., New York, NY.
13. Fyfe, P. K., S. L. Oza, A. H. Fairlamb, and W. N. Hunter 2008. Leishmania trypanothione synthetase-amidase structure reveals a basis for regulation of conflicting synthetic and hydrolytic activities. J. Biol. Chem283:17672- 17680.
14. Galston, A. W., and R. K. Sawhney 1990. Polyamines in plant physiology. Plant Physiol94:406-410.
15. Ghoda, L., M. A. Phillips, K. Bass, C. C. Wang, and P. Coffino 1990. Trypanosome ornithine decarboxylase is stable because it lacks sequences found in the carboxyl terminus of the mouse enzyme which target the latter for intracellular degradation. J. Biol. Chem265:11823-11826.
16. Gibson, W 2007. Resolution of the species problem in African trypanosomes. Int. J. Parasitol37:829-838.
17. Heby, O., S. C. Roberts, and B. Ullman 2003. Polyamine biosynthetic enzymes as drug targets in parasitic protozoa. Biochem. Soc. Trans31:415- 419.
18. Hirumi, H., and K. Hirumi 1989. Continuous cultivation of Trypanosoma brucei blood stream forms in a medium containing a low concentration of serum protein without feeder cell layers. J. Parasitol75:985-989.
19. Huynh, T. T., V. T. Huynh, M. A. Harmon, and M. A. Phillips 2003. Gene knockdown of glutamylcysteine synthetase by RNAi in the parasitic protozoa Trypanosoma brucei demonstrates that it is an essential enzyme. J. Biol. Chem278:39794-39800.
20. Jiang, Y., S. C. Roberts, A. Jardin, N. S. Carter, S. Shih, M. R. Ariyanayagam, A. H. Fairlamb, and B. Ullman 1999. Ornithine decarboxylase gene deletion mutants of Leishmania donovani. J. Biol. Chem274:3781-3788.
21. Kashiwagi, K., S. Miyamoto, F. Suzuki, H. Kobayashi, and K. Igarashi 1992. Excretion of putrescine by the putrescine-ornithine antiporter encoded by the potE gene of Escherichia coli. Proc. Natl. Acad. Sci. USA 89:4529-4533.
22. Kashiwagi, K., R. Pistocchi, S. Shibuya, S. Sugiyama, K. Morikawa, and K. Igarashi 1996. Spermidine-preferential uptake system in Escherichia coli. Identification of amino acids involved in polyamine binding in PotD protein. J. Biol. Chem271:12205-12208.
23. Krieger, S., W. Schwarz, M. R. Ariyanayagam, A. H. Fairlamb, R. L. Krauth- Siegel, and C. Clayton 2000. Trypanosomes lacking trypanothione reductase are avirulent and show increased sensitivity to oxidative stress. Mol. Microbiol. 35:542-552.
24. Li, F., S. Hua, C. C. Wang, and K. Gottesdiener 1998. Trypanosoma brucei brucei: characterization of an ODC null bloodstream form mutant and the action of alpha-difluoromethylornithine. Exp. Parasitol88:255-257.
25. Mangold, U 2006. Antizyme inhibitor: mysterious modulator of cell proliferation. Cell. Mol. Life Sci63:2095-2101.
26. Osterman, A. L., H. B. Brooks, L. K. Jackson, J. J. Abbott, and M. A. Phillips 1999. Lys-69 plays a key role in catalysis by T. bruceiornithine decarboxylase through acceleration of the substrate binding, decarboxylation and product release steps. Biochemistry 38:11814-11826.
27. Pegg, A. E., H. Xiong, D. J. Feith, and L. M. Shantz 1998. S-adenosylmethionine decarboxylase: structure, function and regulation by polyamines. Biochem. Soc. Trans26:580-586.
28. Pegg, A. E 2006. Regulation of ornithine decarboxylase. J. Biol. Chem. 281:14529-14532.
29. Pegg, A. E., and D. J. Feith 2007. Polyamines and neoplastic growth. Biochem. Soc. Trans35:295-299.
30. Phillips, M. A., P. Coffino, and C. C. Wang 1987. Cloning and sequencing of the ornithine decarboxylase gene from Trypanosoma brucei. Implications for enzyme turnover and selective -difluoromethylornithine inhibition. J. Biol. Chem262:8721-8727.
31. Roberts, S., J. Scott, J. Gasteier, Y. Jiang, B. Brooks, A. Jardim, N. Carter, O. Heby, and B. Ullman 2002. S-adenosylmethionine decarboxylase from Leishmania donovani: molecular, genetic and biochemical characterization of null mutants and overproducers. J. Biol. Chem277:5902-5909.
32. Roberts, S. C., Y. Jiang, A. Jardim, N. S. Carter, O. Heby, and B. Ullman 2001. Genetic analysis of spermidine synthase from Leishmania donovani. Mol. Biochem. Parasitol115:217-226.
33. Rodriguez-Caso, C., R. Montanez, M. Cascante, F. Sanchez-Jimenez, and M. A. Medina 2006. Mathematical modeling of polyamine metabolism in mammals. J. Biol. Chem281:21799-21812.
34. Ruan, H., L. M. Shantz, A. E. Pegg, and D. R. Morris 1996. The upstream open reading frame of the mRNA encoding S-adenosylmethionine decar- boxylase is a polyamine-responsive translational control element. J. Biol. Chem271:29576-29582.
35. Taylor, M. C., H. Kaur, B. Blessington, J. M. Kelly, and S. R. Wilkinson 2008. Validation of spermidine synthase as a drug target in African trypanosomes. Biochem. J409:563-569.
36. Uemura, T., H. F. Yerushalmi, G. Tsaprailis, D. E. Stringer, K. E. Pastorian, L. Hawel III, C. V. Byus, and E. W. Gerner 2008. Identification and characterization of a diamine exporter in colon epithelial cells. J. Biol. Chem. 283:26428-26435.
37. Wagner, J., Y. Hirth, N. Claverie, and C. Danzin 1986. A sensitive highperformance liquid chromatographic procedure with fluorometric detection for the analysis of decarboxylated S-adenosylmethionine and analogs in urine samples. Anal. Biochem154:604-617.
38. Wang, Z., J. C. Morris, M. E. Drew, and P. T. Englund 2000. Inhibition of Trypanosoma bruceigene expression by RNA interference using an integratable vector with opposing T7 promoters. J. Biol. Chem275: 40174-40179.
39. Willert, E. K., R. Fitzpatrick, and M. A. Phillips 2007. Allosteric regulation of an essential trypanosome polyamine biosynthetic enzyme by a catalytically dead homolog. Proc. Natl. Acad. Sci. USA 104:8275- 8280.
40. Willert, E. K., and M. A. Phillips 2008. Regulated expression of an essential allosteric activator of polyamine biosynthesis in African trypanosomes. PLoS Pathog4:e1000183.
41. Yarlett, N., and C. J. Bacchi 1988. Effect of DL-alpha- difluoromethylornithine on methionine cycle intermediates in Trypanosoma brucei brucei. Mol. Biochem. Parasitol27:1-10.