Molecular identification and characterization of an essential pyruvate transporter from trypanosoma brucei

Journal of Biological Chemistry

Volumn 288, Issue 20, 2013, Pages 14428-14437

  Sanchez, Marco A ^a  

^a OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GENETIC COMPLEMENTATION; GLUCOSE METABOLISM; MOLECULAR IDENTIFICATION; MULTIGENE FAMILIES; PHYSIOLOGICAL PROCESS; POLYTOPIC PROTEINS; POTENTIAL DRUG TARGETS; TRYPANOSOMA BRUCEI;

MAMMALS; PHYSIOLOGY; YEAST;

GENE EXPRESSION;

CARRIER PROTEINS AND BINDING PROTEINS; MONOCARBOXYLATE TRANSPORTER; PERMEASE; PYRUVIC ACID TRANSPORTER; UNCLASSIFIED DRUG; VEGETABLE PROTEIN;

ARTICLE; BACTERIAL SURVIVAL; BINDING AFFINITY; CELL VIABILITY; CONTROLLED STUDY; DOWN REGULATION; GENE EXPRESSION; GENE IDENTIFICATION; GENETIC COMPLEMENTATION; LIFE CYCLE STAGE; MICROBIAL GROWTH; MOLECULAR CLONING; MULTIGENE FAMILY; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN TARGETING; RNA INTERFERENCE; SACCHAROMYCES CEREVISIAE; TBPT0 GENE; TRYPANOSOMA BRUCEI; UPREGULATION;

CELL DEATH; DRUG TARGET; PARASITE METABOLISM; PYRUVATE; TRANSPORT; TRYPANOSOMA BRUCEI;

AMINO ACID SEQUENCE; BASE SEQUENCE; BIOLOGICAL TRANSPORT; CARBOXYLIC ACIDS; CELL DEATH; CLONING, MOLECULAR; DNA, COMPLEMENTARY; GENE EXPRESSION REGULATION; GENETIC COMPLEMENTATION TEST; MEMBRANE TRANSPORT PROTEINS; MOLECULAR SEQUENCE DATA; PHYLOGENY; PROTOZOAN PROTEINS; RNA INTERFERENCE; SACCHAROMYCES CEREVISIAE; SEQUENCE HOMOLOGY, AMINO ACID; TRYPANOSOMA BRUCEI BRUCEI;

EID: 84877877382     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.473157     Document Type: Article

References (43)

1. Barrett, M. P., and Gilbert, I. H. (2006) Targeting of toxic compounds to the trypanosome's interior. Adv. Parasitol. 63, 125-183 (Pubitemid 44666967)
2. Paulnock, D. M., Freeman, B. E., and Mansfield, J. M. (2010) Modulation of innate immunity by African trypanosomes. Parasitology 137, 2051-2063
3. Bakker, B. M., Westerhoff, H. V., Opperdoes, F. R., and Michels, P. A. (2000) Metabolic control analysis of glycolysis in trypanosomes as an approach to improve selectivity and effectiveness of drugs. Mol. Biochem. Parasitol. 106, 1-10 (Pubitemid 30089205)
4. Opperdoes, F. R., and Michels, P. A. (2001) Enzymes of carbohydrate metabolism as potential drug targets. Int. J. Parasitol. 31, 482-490 (Pubitemid 32382046)
5. Aronov, A. M., Suresh, S., Buckner, F. S., Van Voorhis, W. C., Verlinde, C. L., Opperdoes, F. R., Hol, W. G., and Gelb, M. H. (1999) Structure-based design of submicromolar, biologically active inhibitors of trypanosomatid glyceraldehyde-3-phosphate dehydrogenase. Proc. Natl. Acad. Sci. U.S.A. 96, 4273-4278 (Pubitemid 29190326)
6. Barnard, J. P., Reynafarje, B., and Pedersen, P. L. (1993) Glucose catabolism in African trypanosomes. Evidence that the terminal step is catalyzed by a pyruvate transporter capable of facilitating uptake of toxic analogs. J. Biol. Chem. 268, 3654-3661 (Pubitemid 23071010)
7. Wiemer, E. A., Michels, P. A., and Opperdoes, F. R. (1995) The inhibition of pyruvate transport across the plasma membrane of the bloodstream form of Trypanosoma brucei and its metabolic implications. Biochem. J. 312, 479-484 (Pubitemid 26002214)
8. Halestrap, A. P., Price, N. T. (1999) The proton-linked monocarboxylate transporter (MCT) family: structure, function and regulation. Biochem. J. 343, 281-299 (Pubitemid 29511759)
9. Halestrap, A. P. (2012) The monocarboxylate transporter family-Structure and functional characterization. IUBMB Life 64, 1-9
10. Morris, M. E., and Felmlee, M. A. (2008) Overview of the proton-coupled MCT(SLC16A) family of transporters: characterization, function and role in the transport of the drug of abuse γ-hydroxybutyric acid. AAPS J 10, 311-321
11. Halestrap, A. P., and Wilson, M. C. (2012) The monocarboxylate transporter family-role and regulation. IUBMB Life 64, 109-119
12. Akita, O., Nishimori, C., Shimamoto, T., Fujii, T., and Iefuji, H. (2000) Transport of pyruvate in Saccharomyces cerevisiae and cloning of the gene encoded pyruvate permease. Biosci. Biotechnol. Biochem. 64, 980-984
13. Wiemer, E. A., Ter Kuile, B. H., Michels, P. A., and Opperdoes, F. R. (1992) Pyruvate transport across the plasma membrane of the bloodstream form of Trypanosoma brucei is mediated by a facilitated diffusion carrier. Biochem. Biophys. Res. Commun. 184, 1028-1034
14. Vanderheyden, N., Wong, J., and Docampo, R. (2000) A pyruvate-proton symport and an H+-ATPase regulate the intracellular pH of Trypanosoma brucei at different stages of its life cycle. Biochem. J. 346, 53-62 (Pubitemid 30113819)
15. Sanchez, M. A., Tryon, R., Green, J., Boor, I., and Landfear, S. M. (2002) Six related nucleoside/nucleobase transporters from Trypanosoma brucei exhibit distinct biochemical functions. J. Biol. Chem. 277, 21499-21504 (Pubitemid 34952293)
16. Sunter, J., Wickstead, B., Gull, K., and Carrington, M. (2012) A new generation of T7 RNA polymerase-independent inducible expression plasmids for Trypanosoma brucei. PLoS One 7, e35167
17. van Deursen, F. J., Shahi, S. K., Turner, C. M., Hartmann, C., Guerra- Giraldez, C., Matthews, K. R., and Clayton, C. E. (2001) Characterisation of the growth and differentiation in vivo and in vitro-of bloodstream-form Trypanosoma brucei strain TREU 927. Mol. Biochem. Parasitol. 112, 163-171 (Pubitemid 32167093)
18. Ortiz, D., Sanchez, M. A., Quecke, P., and Landfear, S. M. (2009) Two novel nucleobase/pentamidine transporters from Trypanosoma brucei. Mol. Biochem. Parasitol. 163, 67-76
19. Sambrook, J., Fritsch, E. F., and Maniatis, T (1989) Molecular Cloning: A Laboratory Manual, pp. 7.37-7.52, Cold Spring Harbor Laboratory, Cold Spring Harbor, NY
20. Makuc, J., Cappellaro, C., and Boles, E. (2004) Co-expression of a mammalian accessory trafficking protein enables functional expression of the rat MCT1 monocarboxylate transporter in Saccharomyces cerevisiae. FEMS Yeast Res. 4, 795-801 (Pubitemid 39140649)
21. Mazhari-Tabrizi, R., Eckert, V., Blank, M., Müller, R., Mumberg, D., Funk, M., and Schwarz, R. T. (1996) Cloning and functional expression of glycosyltransferases from parasitic protozoans by heterologous complementation in yeast: the dolichol phosphate mannose synthase from Trypanosoma brucei brucei. Biochem. J. 316, 853-858 (Pubitemid 26278437)
22. Sanchez, M. A., Drutman, S., van Ampting, M., Matthews, K., and Landfear, S. M. (2004) A novel purine nucleoside transporter whose expression is up-regulated in the short stumpy form of the Trypanosoma brucei life cycle. Mol. Biochem. Parasitol. 136, 265-272 (Pubitemid 38757995)
23. Cheng, Y., and Prusoff, W. H. (1973) Relationship between the inhibition constant (K1) and the concentration of inhibitor which causes 50 per cent inhibition (I50) of an enzymatic reaction. Biochem. Pharmacol. 22, 3099-3108
24. Mäser, P., Sütterlin, C., Kralli, A., and Kaminsky, R. (1999) A nucleoside transporter from Trypanosoma brucei involved in drug resistance. Science 285, 242-244 (Pubitemid 29329994)
25. Van Hellemond, J. J., Neuville, P., Schwarz, R. T., Matthews, K. R., and Mottram, J. C. (2000) Isolation of Trypanosoma brucei CYC2 and CYC3 cyclin genes by rescue of a yeast G(1) cyclin mutant. Functional characterization of CYC2. J. Biol. Chem. 275, 8315-8323 (Pubitemid 30180171)
26. Brems, S., Guilbride, D. L., Gundlesdodjir-Planck, D., Busold, C., Luu, V. D., Schanne, M., Hoheisel, J., and Clayton, C. (2005) The transcriptomes of Trypanosoma brucei Lister 427 and TREU927 bloodstream and procyclic trypomastigotes. Mol. Biochem. Parasitol. 139, 163-172 (Pubitemid 40128212)
27. Queiroz, R., Benz, C., Fellenberg, K., Hoheisel, J. D., and Clayton, C. (2009) Transcriptome analysis of differentiating trypanosomes reveals the existence of multiple post-transcriptional regulons. BMC Genomics 10, 495
28. Jensen, B. C., Sivam, D., Kifer, C. T., Myler, P. J., and Parsons, M. (2009) Widespread variation in transcript abundance within and across developmental stages of Trypanosoma brucei. BMC Genomics 10, 482
29. Veitch, N. J., Johnson, P. C., Trivedi, U., Terry, S., Wildridge, D., and MacLeod, A. (2010) Digital gene expression analysis of two life cycle stages of the human-infective parasite, Trypanosoma brucei gambiense reveals differentially expressed clusters of co-regulated genes. BMCGenomics 11, 124
30. Siegel, T. N., Hekstra, D. R., Wang, X., Dewell, S., and Cross, G. A. (2010) Genome-wide analysis of mRNA abundance in two life-cycle stages of Trypanosoma brucei and identification of splicing and polyadenylation sites. Nucleic Acids Res. 38, 4946-4957
31. Choi, W. G., and Roberts, D. M. (2007) Arabidopsis NIP2;1, a major intrinsic protein transporter of lactic acid induced by anoxic stress. J. Biol. Chem. 282, 24209-24218
32. Nolan, D. P., and Voorheis, H. P. (2000) Factors that determine the plasma-membrane potential in bloodstream forms of Trypanosoma brucei. Eur. J. Biochem. 267, 4615-4623 (Pubitemid 30619450)
33. Alsford, S., Turner, D. J., Obado, S. O., Sanchez-Flores, A., Glover, L., Berriman, M., Hertz-Fowler, C., and Horn, D. (2011) High-throughput phenotyping using parallel sequencing of RNA interference targets in the African trypanosome. Genome Res. 21, 915-924
34. Barnard, J. P., and Pedersen, P. L. (1994) Alteration of pyruvate metabolism in African trypanosomes during differentiation from bloodstream into insect forms. Arch Biochem. Biophys. 313, 77-82 (Pubitemid 24261093)
35. Haanstra, J. R., Kerkhoven, E. J., van Tuijl, A., Blits, M., Wurst, M., van Nuland, R., Albert, M. A., Michels, P. A., Bouwman, J., Clayton, C., Westerhoff, H. V., and Bakker, B. M. (2011) A domino effect in drug action: from metabolic assault towards parasite differentiation. Mol. Microbiol. 79, 94-108
36. Tielens, A. G., and van Hellemond, J. J. (2009) Surprising variety in energy metabolism within Trypanosomatidae. Trends Parasitol. 25, 482-490
37. +/lactate cotransporter (MCT1). Biochemical Journal 320, 817-824
38. Hannaert, V., Bringaud, F., Opperdoes, F. R., and Michels, P. A. (2003) Evolution of energy metabolism and its compartmentation in Kinetoplastida. Kinetoplastid. Biol. Dis. 2, 11
39. Hannaert, V., Saavedra, E., Duffieux, F., Szikora, J. P., Rigden, D. J., Michels, P. A., and Opperdoes, F. R. (2003) Plant-like traits associated with metabolism of Trypanosoma parasites. Proc. Natl. Acad. Sci. U.S.A. 100, 1067-1071 (Pubitemid 36183956)
40. Dean, S., Marchetti, R., Kirk, K., and Matthews, K. R. (2009) A surface transporter family conveys the trypanosome differentiation signal. Nature 459, 213-217
41. Merezhinskaya, N., and Fishbein, W. N. (2009) Monocarboxylate transporters: past, present, and future. Histol. Histopathol. 24, 243-264
42. Urbaniak, M. D., Guther, M. L., and Ferguson, M. A. (2012) Comparative SILAC proteomic analysis of Trypanosoma brucei bloodstream and procyclic lifecycle stages. PLoS One 7, e36619
43. Butter, F., Bucerius, F., Michel, M., Cicova, Z., Mann, M., and Janzen, C. J. (2013) Comparative proteomics of two life cycle stages of stable isotope-labeled Trypanosoma brucei reveals novel components of the parasite's host adaptation machinery. Mol. Cell Proteomics 12, 172-179