Role of hexosamine biosynthesis in Leishmania growth and virulence

Molecular Microbiology

Volumn 69, Issue 4, 2008, Pages 858-869

  Naderer, Thomas ^a   Wee, Edmund ^a   McConville, Malcolm J ^a  

^a UNIVERSITY OF MELBOURNE   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

DOLICHOL; GLUTAMINE FRUCTOSE 6 PHOSPHATE AMINOTRANSFERASE; GLYCOCONJUGATE; GLYCOSYLPHOSPHATIDYLINOSITOL; HEXOSAMINE; N ACETYLGLUCOSAMINE; OLIGOSACCHARIDE; TUNICAMYCIN;

AMASTIGOTE; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BIOSYNTHESIS; CONTROLLED STUDY; FEMALE; HEAT TOLERANCE; LEISHMANIA MAJOR; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PARASITE VIRULENCE; PHAGOLYSOSOME; PRIORITY JOURNAL; PROMASTIGOTE; PROTEIN ANALYSIS; PROTOZOAL INFECTION; STARVATION; TEMPERATURE SENSITIVITY; WILD TYPE;

ACETYLGLUCOSAMINE; AMINO ACID SEQUENCE; ANIMALS; GENE DELETION; GENES, PROTOZOAN; GLUTAMINE-FRUCTOSE-6-PHOSPHATE TRANSAMINASE (ISOMERIZING); LEISHMANIA MAJOR; LEISHMANIASIS, CUTANEOUS; MICE; MOLECULAR SEQUENCE DATA; VIRULENCE;

LEISHMANIA MAJOR; MAMMALIA; MUS;

EID: 47749148417     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2008.06314.x     Document Type: Article

References (51)

1. Alvarez, F.J. Konopka, J.B. (2007) Identification of an N-acetylglucosamine transporter that mediates hyphal induction in Candida albicans. Mol Biol Cell 18 : 965 975.
2. Antoine, J.C., Prina, E., Courret, N. Lang, T. (2004) Leishmania spp. on the interactions they establish with antigen-presenting cells of their mammalian hosts. Adv Parasitol 58 : 1 68.
3. Banerjee, S., Vishwanath, P., Cui, J., Kelleher, D.J., Gilmore, R., Robbins, P.W. Samuelson, J. (2007) The evolution of N-glycan-dependent endoplasmic reticulum quality control factors for glycoprotein folding and degradation. Proc Natl Acad Sci USA 104 : 11676 11681.
4. Bause, E., Breuer, W. Peters, S. (1995) Investigation of the active site of oligosaccharyltransferase from pig liver using synthetic tripeptides as tools. Biochem J 312 (Part 3 979 985.
5. Burchmore, R.J., Rodriguez-Contreras, D., McBride, K., Merkel, P., Barrett, M.P., Modi, G., et al. (2003) Genetic characterization of glucose transporter function in Leishmania mexicana. Proc Natl Acad Sci USA 100 : 3901 3906.
6. Capul, A.A., Hickerson, S., Barron, T., Turco, S.J. Beverley, S.M. (2007) Comparisons of mutants lacking the Golgi UDP-galactose or GDP-mannose transporters establish that phosphoglycans are important for promastigote but not amastigote virulence in Leishmania major. Infect Immun 75 : 4629 4637.
7. Chen, D.Q., Lu, H. Chang, K.P. (1999) Replacement of Leishmania N-acetylglucosamine-1-phosphate transferase gene requires episomal rescue. Mol Biochem Parasitol 100 : 223 227.
8. Conte, I., Labriola, C., Cazzulo, J.J., Docampo, R. Parodi, A.J. (2003) The interplay between folding-facilitating mechanisms in Trypanosoma cruzi endoplasmic reticulum. Mol Biol Cell 14 : 3529 3540.
9. Croft, S.L. Coombs, G.H. (2003) Leishmaniasis - current chemotherapy and recent advances in the search for novel drugs. Trends Parasitol 19 : 502 508.
10. Davies, C.R., Kaye, P., Croft, S.L. Sundar, S. (2003) Leishmaniasis: new approaches to disease control. BMJ 326 : 377 382.
11. Ebikeme, C.E., Peacock, L., Coustou, V., Riviere, L., Bringaud, F., Gibson, W.C. Barrett, M.P. (2008) N-acetyl d-glucosamine stimulates growth in procyclic forms of Trypanosoma brucei by inducing a metabolic shift. Parasitology 135 : 585 594.
12. Elbein, A.D. (1987) Inhibitors of the biosynthesis and processing of N-linked oligosaccharide chains. Annu Rev Biochem 56 : 497 534.
13. Funk, V.A., Thomas-Oates, J.E., Kielland, S.L., Bates, P.A. Olafson, R.W. (1997) A unique, terminally glucosylated oligosaccharide is a common feature on Leishmania cell surfaces. Mol Biochem Parasitol 84 : 33 48.
14. Garami, A. Ilg, T. (2001) Disruption of mannose activation in Leishmania mexicana: GDP-mannose pyrophosphorylase is required for virulence, but not for viability. EMBO J 20 : 3657 3666.
15. Garami, A., Mehlert, A. Ilg, T. (2001) Glycosylation defects and virulence phenotypes of Leishmania mexicana phosphomannomutase and dolicholphosphate-mannose synthase gene deletion mutants. Mol Cell Biol 21 : 8168 8183.
16. Gibbs, B.S. Coward, J.K. (1999) Dolichylpyrophosphate oligosaccharides: large-scale isolation and evaluation as oligosaccharyltransferase substrates. Bioorg Med Chem 7 : 441 447.
17. Handman, E., Barnett, L.D., Osborn, A.H., Goding, J.W. Murray, P.J. (1993) Identification, characterisation and genomic cloning of a O-linked N-acetylglucosamine-containing cytoplasmic Leishmania glycoprotein. Mol Biochem Parasitol 62 : 61 72.
18. Hilley, J.D., Zawadzki, J.L., McConville, M.J., Coombs, G.H. Mottram, J.C. (2000) Leishmania mexicana mutants lacking glycosylphosphatidylinositol (GPI): protein transamidase provide insights into the biosynthesis and functions of GPI-anchored proteins. Mol Biol Cell 11 : 1183 1195.
19. Hsiao, C.H., Yao, C., Storlie, P., Donelson, J.E. Wilson, M.E. (2008) The major surface protease (MSP or GP63) in the intracellular amastigote stage of Leishmania chagasi. Mol Biochem Parasitol 157 : 148 159.
20. Hubel, A., Krobitsch, S., Horauf, A. Clos, J. (1997) Leishmania major Hsp100 is required chiefly in the mammalian stage of the parasite. Mol Cell Biol 17 : 5987 5995.
21. Ilg, T., Overath, P., Ferguson, M.A., Rutherford, T., Campbell, D.G. McConville, M.J. (1994) O- and N-glycosylation of the Leishmania mexicana-secreted acid phosphatase. Characterization of a new class of phosphoserine-linked glycans. J Biol Chem 269 : 24073 24081.
22. Ilgoutz, S.C., Zawadzki, J.L., Ralton, J.E. McConville, M.J. (1999) Evidence that free GPI glycolipids are essential for growth of Leishmania mexicana. EMBO J 18 : 2746 2755.
23. Ivens, A.C., Peacock, C.S., Worthey, E.A., Murphy, L., Aggarwal, G., Berriman, M., et al. (2005) The genome of the kinetoplastid parasite, Leishmania major. Science 309 : 436 424.
24. Jones, D.C., Mehlert, A., Guther, M.L. Ferguson, M.A. (2005) Deletion of the glucosidase II gene in Trypanosoma brucei reveals novel N-glycosylation mechanisms in the biosynthesis of variant surface glycoprotein. J Biol Chem 280 : 35929 35942.
25. Kamiya, Y., Kamiya, D., Yamamoto, K., Nyfeler, B., Hauri, H.P. Kato, K. (2008) Molecular basis of sugar recognition by the human 1-type lectins ERGIC-53, VIPL, and VIP36. J Biol Chem 283 : 1857 1861.
26. Kedzierski, L., Malby, R.L., Smith, B.J., Perugini, M.A., Hodder, A.N., Ilg, T., et al. (2006) Structure of Leishmania mexicana phosphomannomutase highlights similarities with human isoforms. J Mol Biol 363 : 215 227.
27. Kink, J.A. Chang, K.P. (1987) Tunicamycin-resistant Leishmania mexicana amazonensis: expression of virulence associated with an increased activity of N-acetylglucosaminyltransferase and amplification of its presumptive gene. Proc Natl Acad Sci USA 84 : 1253 1257.
28. Labriola, C., Cazzulo, J.J. Parodi, A.J. (1995) Retention of glucose units added by the UDP-GLC: glycoprotein glucosyltransferase delays exit of glycoproteins from the endoplasmic reticulum. J Cell Biol 130 : 771 779.
29. Labriola, C., Cazzulo, J.J. Parodi, A.J. (1999) Trypanosoma cruzi calreticulin is a lectin that binds monoglucosylated oligosaccharides but not protein moieties of glycoproteins. Mol Biol Cell 10 : 1381 1394.
30. Langford, C.K., Kavanaugh, M.P., Stenberg, P.E., Drew, M.E., Zhang, W. Landfear, S.M. (1995) Functional expression and subcellular localization of a high-Km hexose transporter from Leishmania donovani. Biochemistry 34 : 11814 11821.
31. Liu, X. Chang, K.P. (1992) The 63-kilobase circular amplicon of tunicamycin-resistant Leishmania amazonensis contains a functional N-acetylglucosamine-1-phosphate transferase gene that can be used as a dominant selectable marker in transfection. Mol Cell Biol 12 : 4112 4122.
32. McConville, M.J., Mullin, K.A., Ilgoutz, S.C. Teasdale, R.D. (2002) Secretory pathway of trypanosomatid parasites. Microbiol Mol Biol Rev 66 : 122 154.
33. McConville, M.J., de Souza, D., Saunders, E., Likic, V.A. Naderer, T. (2007) Living in a phagolysosome; metabolism of Leishmania amastigotes. Trends Parasitol 23 : 368 375.
34. Milewski, S. (2002) Glucosamine-6-phosphate synthase - the multi-facets enzyme. Biochim Biophys Acta 1597 : 173 192.
35. Milewski, S., Gabriel, I. Olchowy, J. (2006) Enzymes of UDP-GlcNAc biosynthesis in yeast. Yeast 23 : 1 14.
36. Naderer, T. McConville, M.J. (2008) The Leishmania-macrophage interaction: a metabolic perspective. Cell Microbiol 10 : 301 308.
37. Naderer, T., Vince, J.E. McConville, M.J. (2004) Surface determinants of Leishmania parasites and their role in infectivity in the mammalian host. Curr Mol Med 4 : 649 665.
38. Naderer, T., Ellis, M.A., Sernee, M.F., De Souza, D.P., Curtis, J., Handman, E. McConville, M.J. (2006) Virulence of Leishmania major in macrophages and mice requires the gluconeogenic enzyme fructose-1,6-bisphosphatase. Proc Natl Acad Sci USA 103 : 5502 5507.
39. Nolan, T.J. Farrell, J.P. (1985) Inhibition of in vivo and in vitro infectivity of Leishmania donovani by tunicamycin. Mol Biochem Parasitol 16 : 127 135.
40. Olchowy, J., Kur, K., Sachadyn, P. Milewski, S. (2006) Construction, purification, and functional characterization of His-tagged Candida albicans glucosamine-6-phosphate synthase expressed in Escherichia coli. Protein Expr Purif 46 : 309 315.
41. Parodi, A.J. (1993) N-glycosylation in trypanosomatid protozoa. Glycobiology 3 : 193 199.
42. Ralton, J.E. McConville, M.J. (1998) Delineation of three pathways of glycosylphosphatidylinositol biosynthesis in Leishmania mexicana. Precursors from different pathways are assembled on distinct pools of phosphatidylinositol and undergo fatty acid remodeling. J Biol Chem 273 : 4245 4257.
43. Ralton, J.E., Naderer, T., Piraino, H.L., Bashtannyk, T.A., Callaghan, J.M. McConville, M.J. (2003) Evidence that intracellular β1-2 mannan is a virulence factor in Leishmania parasites. J Biol Chem 278 : 40757 40763.
44. Samuelson, J., Banerjee, S., Magnelli, P., Cui, J., Kelleher, D.J., Gilmore, R. Robbins, P.W. (2005) The diversity of dolichol-linked precursors to Asn-linked glycans likely results from secondary loss of sets of glycosyltransferases. Proc Natl Acad Sci USA 102 : 1548 1553.
45. Schneider, P., Rosat, J.P., Ransijn, A., Ferguson, M.A. McConville, M.J. (1993) Characterization of glycoinositol phospholipids in the amastigote stage of the protozoan parasite Leishmania major. Biochem J 295 (Part 2 555 564.
46. Spath, G.F., Garraway, L.A., Turco, S.J. Beverley, S.M. (2003) The role(s) of lipophosphoglycan (LPG) in the establishment of Leishmania major infections in mammalian hosts. Proc Natl Acad Sci USA 100 : 9536 9541.
47. Stokes, M., Guther, M., Turnock, D., Prescott, A., Martin, K., Alphey, M. Ferguson, M. (2008) Then synthesis of UDP-N-acetylglucosamine is essential for bloodstream form Trypanosoma brucei in vitro and in vivo and UDP-N-acetylglucosamine starvation reveals a hierachy in parasite protein glycosylation. J Biol Chem 283 : 16147 16161.
48. Titus, R.G., Marchand, M., Boon, T. Louis, J.A. (1985) A limiting dilution assay for quantifying Leishmania major in tissues of infected mice. Parasite Immunol 7 : 545 555.
49. Turco, S.J., Spath, G.F. Beverley, S.M. (2001) Is lipophosphoglycan a virulence factor? A surprising diversity between Leishmania species. Trends Parasitol 17 : 223 226.
50. van Zandbergen, G., Klinger, M., Mueller, A., Dannenberg, S., Gebert, A., Solbach, W. Laskay, T. (2004) Cutting edge: neutrophil granulocyte serves as a vector for Leishmania entry into macrophages. J Immunol 173 : 6521 6525.
51. Zufferey, R., Allen, S., Barron, T., Sullivan, D.R., Denny, P.W., Almeida, I.C., et al. (2003) Ether phospholipids and glycosylinositolphospholipids are not required for amastigote virulence or for inhibition of macrophage activation by Leishmania major. J Biol Chem 278 : 44708 44718.