Substrate specificity of the Leishmania donovani myo-inositol transporter: Critical role of inositol C-2, C-3 and C-5 hydroxyl groups

Molecular and Biochemical Parasitology

Volumn 135, Issue 1, 2004, Pages 133-141

  Mongan, Tyler P ^a   Ganapasam, Sudhandiran ^a   Hobbs, Stephen B ^a   Seyfang, Andreas ^a  

^a MEDICAL COLLEGE OF GEORGIA   (United States)

Author keywords

3 fluoro 3 deoxy myo inositol; 3F Ins; Glycosyl phosphatidylinositol; GPI; Leishmania myo inositol transport; Mammalian sodium coupled myo inositol transporter; MIT; myo inositol transporter of L. donovani; PBS; Phosphate buffered saline; SMIT

Indexed keywords

FLUOROINOSITOL; HYDROXYL GROUP; INOSITOL DERIVATIVE; UNCLASSIFIED DRUG;

ARTICLE; CELL GROWTH; CELL PROLIFERATION; CONCENTRATION RESPONSE; CONTROLLED STUDY; DRUG EFFECT; ENZYME SPECIFICITY; ENZYME SUBSTRATE; GROWTH INHIBITION; IC 50; LEISHMANIA DONOVANI; NONHUMAN; PRIORITY JOURNAL; PROMASTIGOTE; TRANSPORT KINETICS;

ANIMALS; ANTIPROTOZOAL AGENTS; BIOLOGICAL TRANSPORT; FUCOSE; HYDROGEN-ION CONCENTRATION; INOSITOL; LEISHMANIA DONOVANI; MEMBRANE PROTEINS; MEMBRANE TRANSPORT PROTEINS; MONOSACCHARIDES; PROTOZOAN PROTEINS; STEREOISOMERISM; SUBSTRATE SPECIFICITY; XYLOSE;

LEISHMANIA DONOVANI; MAMMALIA;

EID: 1842763132     PISSN: 01666851     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.molbiopara.2004.01.015     Document Type: Article

References (54)

1. Pearson RD, Jeronimo SMB, de Queiroz Sousa A. Leishmaniasis. In: Guerrant RL, Walker DH, Weller PF, editors. Tropical infectious diseases: principles, pathogens, and practice. Philadelphia: Churchill Livingstone; 1999. p. 797-813.
2. de Gorgolas M., Miles M.A. Visceral leishmaniasis and AIDS. Nature. 372:1994;734.
3. Alvar J., Cañavate C., Gutiérrez-Solar B.et al. Leishmania and human immunodeficiency virus coinfection: the first 10 years. Clin. Microbiol. Rev. 10:1997;298-319.
4. Enserink M. Has leishmaniasis become endemic in the US? Science. 290:2000;188-189.
5. McConville M.J., Ferguson M.A.J. The structure, biosynthesis and function of glycosylated phosphatidylinositols in the parasitic protozoa and higher eukaryotes. Biochem. J. 294:1993;305-324.
6. McConville M.J., Menon A.K. Recent developments in the cell biology and biochemistry of glycosylphosphatidylinositol lipids. Mol. Membr. Biol. 17:2000;1-16.
7. Chang C.S., Chang K.-P. Monoclonal antibody affinity purification of a Leishmania membrane glycoprotein and its inhibition of leishmania-macrophage binding. Proc. Natl. Acad Sci. U.S.A. 83:1986;100-104.
8. Russell D.G., Wilhelm H. The involvement of the major surface glycoprotein (gp63) of Leishmania promastigotes in attachment to macrophages. J. Immunol. 136:1986;2613-2620.
9. Descoteaux A., Turco S.J. Functional aspects of the Leishmania donovani lipophosphoglycan during macrophage infection. Microbes Infect. 4:2002;975-981.
10. Sacks D.L., Modi G., Rowton E.et al. The role of phosphoglycans in Leishmania-sand fly interactions. Proc. Natl. Acad. Sci. U.S.A. 97:2000;406-411.
11. + symporter from Leishmania donovani. Mol. Cell Biol. 15:1995;5508-5515.
12. + symporter from Leishmania donovani. J. Biol. Chem. 272:1997;24210-24215.
13. + symporter. J. Biol. Chem. 275:2000;5687-5693.
14. Klamo E.M., Drew M.E., Landfear S.M., Kavanaugh M.P. Kinetics and stoichiometry of a proton/myo-inositol cotransporter. J. Biol. Chem. 271:1996;14937-14943.
15. Zilberstein D., Dwyer D.M. Protonmotive force-driven active transport of D-glucose and L-proline in the protozoan parasite Leishmania donovani. Proc. Natl. Acad. Sci. U.S.A. 82:1985;1716-1720.
16. Stein A., Vasudevan G., Carter N.S., Ullman B., Landfear S.M., Kavanaugh M.P. Equilibrative nucleoside transporter family members from Leishmania donovani are electrogenic proton symporters. J. Biol. Chem. 278:2003;35127- 35134.
17. Henderson P.J.F. Sugar transport proteins. Curr. Opin. Struct. Biol. 1:1991;590-601.
18. Baldwin S.A. Mammalian passive glucose transporters: members of an ubiquitous family of active and passive transport proteins. Biochim. Biophys. Acta. 1154:1993;17-49.
19. Seyfang A, Landfear SM. Targeted gene disruption of the Leishmania donovani myo-inositol transporter MIT. Molecular Parasitology Meeting IX, Woods Hole, MA. Abstracts 2000:78.
20. Ilg T. Generation of myo-inositol-auxotrophic Leishmania mexicana mutants by targeted replacement of the myo-inositol-1-phosphate synthase gene. Mol. Biochem. Parasitol. 120:2002;151-156.
21. Seyfang A., Landfear S.M. Substrate depletion upregulates uptake of myo-inositol, glucose and adenosine in Leishmania. Mol. Biochem. Parasitol. 104:1999;121-130.
22. +/myo-inositol cotransporter, a hypertonicity stress protein. J. Biol. Chem. 267:1992;6297-6301.
23. +/myo-inositol cotransporter. J. Biol. Chem. 277:2002;35219-35224.
24. Reizer J., Reizer A., Saier M.H. Jr. A functional superfamily of sodium/solute symporters. Biochim. Biophys. Acta. 1197:1994;133-166.
25. Turk E., Wright E.M. Membrane topology motifs in SGLT cotransporter family. J. Membr. Biol. 159:1997;1-20.
26. Schlein Y. Sandfly diet and Leishmania. Parasitol. Today. 2:1986;175-177.
27. Hamilton J.G., El Naiem D.A. Sugars in the gut of the sandfly Phlebotomus orientalis from Dinder National Park, Eastern Sudan. Med. Vet. Entomol. 14:2000;64-70.
28. Zar JH. Paired-sample hypotheses. In: Biostatistical analysis. 4th ed. Upper Saddle River, NJ: Prentice-Hall; 1999. p. 161-76.
29. Bisswanger H. Analysis of enzyme kinetic data. In: Enzyme kinetics: principles and methods. Weinheim, Germany: Wiley-VCH; 2002. p. 58-75.
30. Sima A.A., Dunlap J.A., Davidson E.P.et al. Supplemental myo-inositol prevents L-fucose-induced diabetic neuropathy. Diabetes. 46:1997;301-306.
31. +/myo-inositol cotransporter expressed in Xenopus oocytes. J. Membr. Biol. 143:1995;103-113.
32. Kerovuo J., Rouvinen J., Hatzack F. Analysis of myo-inositol hexakisphosphate hydrolysis by Bacillus phytase: indication of a novel reaction mechanism. Biochem. J. 352:2000;623-628.
33. Nikawa J., Tsukagoshi Y., Yamashita S. Isolation and characterization of two distinct myo-inositol transporter genes of Saccharomyces cerevisiae. J. Biol. Chem. 266:1991;11184-11191.
34. Lai K., McGraw P. Dual control of inositol transport in Saccharomyces cerevisiae by irreversible inactivation of permease and regulation of permease synthesis by INO2, INO4, and OPI1. J. Biol. Chem. 269:1994;2245-2251.
35. Cheneval J.P., Deshusses J., Posternak T. Sur le transport de l'inositol chez Schizosaccharomyces pombe. Biochim. Biophys. Acta. 203:1970;348-350.
36. Jin J.H., Seyfang A. High-affinity myo-inositol transport in Candida albicans: substrate specificity and pharmacology. Microbiology. 149:2003;3371-3381.
37. Glaser T.A., Utz G.L., Mukkada A.J. The plasma membrane electrical gradient (membrane potential) in Leishmania donovani promastigotes and amastigotes. Mol. Biochem. Parasitol. 51:1992;9-16.
38. + pumping by Leishmania major promastigotes. J. Biol. Chem. 270:1995;5299-5304.
39. Matskevitch J., Wagner C.A., Risler T.et al. Effect of extracellular pH on the myo-inositol transporter SMIT expressed in Xenopus oocytes. Eur. J. Physiol. 436:1994;854-857.
40. Powis G., Aksoy I.A., Melder D.C.et al. D-3-Deoxy-3-substituted myo-inositol analogues as inhibitors of cell growth. Cancer Chemother. Pharmacol. 29:1991;95-104.
41. 3H -labelled monodeoxyfluoro-myo-inositols into thymocytes and their incorporation into phospholipid in permeabilized cells Biochem. J. 291:1993;553-560.
42. Johnson S.C., Dahl J., Shih T.-L.et al. Synthesis and evaluation of 3-modified 1 D-myo-inositols as inhibitors and substrates of phosphatidylinositol synthase and inhibitors of myo-inositol uptake by cells. J. Med. Chem. 36:1993;3628-3635.
43. Wiedemann C., Cockcroft S. Vesicular transport: sticky fingers grab a lipid. Nature. 394:1998;426-427.
44. Simonsen A., Wurmser A.E., Emr S.E., Stenmark H. The role of phosphoinositides in membrane transport. Curr. Opin. Cell Biol. 13:2001;485-492.
45. Berridge M.J. Inositol trisphosphate and calcium signalling. Nature. 264:1993;1274-1283.
46. Späth G.F., Epstein L., Leader B.et al. Lipophosphoglycan is a virulence factor distinct from related glycoconjugates in the protozoan parasite Leishmania major. Proc. Natl. Acad. Sci. U.S.A. 97:2000;9258-9263.
47. Späth G.F., Lye L.F., Segawa H., Sacks D.L., Turco S.J., Beverley S.M. Persistence without pathology in phosphoglycan-deficient Leishmania major. Science. 301:2003;1241-1243.
48. Ostlund R.E. Jr., McGill J.B., Herskowitz I., Kipnis D.M., Santiago J.V., Sherman W.R. D-chiro-Inositol metabolism in diabetes mellitus. Proc. Natl. Acad. Sci. U.S.A. 90:1993;9988-9992.
49. Kouzuma T., Takahashi M., Endoh T., Kaneko R., Ura N., Shimamoto K.et al. An enzymatic cycling method for the measurement of myo-inositol in biological samples. Clin. Chim. Acta. 312:2001;143-151.
50. Lentner C. Cerebrospinal fluid. In: Geigy scientific tables, vol. 1: body fluids. Basle, Switzerland: Ciba-Geigy Ltd.; 1981. p. 165-77.
51. Harrison J.F. Insect acid-base physiology. Annu. Rev. Entomol. 46:2001;221-250.
52. Linger M., Acosta-Serrano A., Van Den Abbeele J., Kunz Renggli C., Brun R., Englund P.T.et al. Cleavage of trypanosome surface glycoproteins by alkaline trypsin-like enzyme(s) in the midgut of Glossina morsitans. Int. J. Parasitol. 33:2003;1319-1328.
53. Dillon R.J., Lane R.P. Bloodmeal digestion in the midgut of Phlebotomus papatasi and Phlebotomus langeroni. Med. Vet. Entomol. 7:1993;225-232.
54. +-myo-inositol symporter expressed predominantly in the brain. EMBO J. 20:2001;4467-4477.