Leishmania major lacking arginase (ARG) are auxotrophic for polyamines but retain infectivity to susceptible BALB/c mice

Molecular and Biochemical Parasitology

Volumn 165, Issue 1, 2009, Pages 48-56

  Reguera, Rosa M ^a   Balaña Fouce, Rafael ^a   Showalter, Melissa ^b   Hickerson, Suzanne ^b   Beverley, Stephen M ^b  

^a UNIVERSITY OF LEÓN   (Spain)

^b WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Infections; l arginine; l ornithine; Nitric oxide; Null mutant; Polyamines; Trypanosomatid protozoan

Indexed keywords

ARGINASE; EFLORNITHINE; N(G) HYDROXYARGININE; ORNITHINE; POLYAMINE DERIVATIVE;

ANIMAL MODEL; ARTICLE; BAGG ALBINO MOUSE; CONTROLLED STUDY; CULTURE TECHNIQUE; ENZYME ACTIVITY; GENE TARGETING; HOST SUSCEPTIBILITY; IN VITRO STUDY; INFECTION; INOCULATION; LEISHMANIA MAJOR; MOUSE; MUTANT; NONHUMAN; PRIORITY JOURNAL; PROMASTIGOTE; PROTEIN EXPRESSION; SYNTHESIS; WILD TYPE;

AMINO ACIDS; ANIMALS; ARGINASE; ENZYME INHIBITORS; GENE EXPRESSION; INTRACELLULAR SPACE; LEISHMANIA MAJOR; MICE; MICE, INBRED BALB C; ORNITHINE; PARASITIC SENSITIVITY TESTS; POLYAMINES;

EUKARYOTA; LEISHMANIA MAJOR; MUS; PROTOZOA; TRYPANOSOMATIDAE;

EID: 60649087303     PISSN: 01666851     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.molbiopara.2009.01.001     Document Type: Article

References (47)

1. Morris Jr. S.M. Arginine: beyond protein. Am J Clin Nutr 83 (2006) 508S-512S
2. MacMicking J., Xie Q.W., and Nathan C. Nitric oxide and macrophage function. Annu Rev Immunol 15 (1997) 323-350
3. Modolell M., Corraliza I.M., Link F., Soler G., and Eichmann K. Reciprocal regulation of the nitric oxide synthase/arginase balance in mouse bone marrow-derived macrophages by TH1 and TH2 cytokines. Eur J Immunol 25 (1995) 1101-1104
4. Peranzoni E., Marigo I., Dolcetti L., et al. Role of arginine metabolism in immunity and immunopathology. Immunobiology 212 (2007) 795-812
5. Bronte V., and Zanovello P. Regulation of immune responses by L-arginine metabolism. Nat Rev Immunol 5 (2005) 641-654
6. Iniesta V., Gomez-Nieto L.C., and Corraliza I. The inhibition of arginase by N(omega)-hydroxy-l-arginine controls the growth of Leishmania inside macrophages. J Exp Med 193 (2001) 777-784
7. Wanasen N., and Soong L. L-arginine metabolism and its impact on host immunity against Leishmania infection. Immunol Res 41 (2008) 15-25
8. Jenkinson C.P., Grody W.W., and Cederbaum S.D. Comparative properties of arginases. Comp Biochem Physiol B Biochem Mol Biol 114 (1996) 107-132
9. Ash D.E. Structure and function of arginases. J Nutr 134 (2004) 2760S-2767S
10. Mori M., and Gotoh T. Arginine metabolic enzymes, nitric oxide and infection. J Nutr 134 (2004) 2820S-2825S
11. da Silva E.R., Castilho T.M., Pioker F.C., Tomich de Paula Silva C.H., and Floeter-Winter L.M. Genomic organisation and transcription characterisation of the gene encoding Leishmania (Leishmania) amazonensis arginase and its protein structure prediction. Int J Parasitol 32 (2002) 727-737
12. Roberts S.C., Tancer M.J., Polinsky M.R., Gibson K.M., Heby O., and Ullman B. Arginase plays a pivotal role in polyamine precursor metabolism in Leishmania. Characterization of gene deletion mutants. J Biol Chem 279 (2004) 23668-23678
13. da Silva E.R., da Silva M.F., Fischer H., et al. Biochemical and biophysical properties of a highly active recombinant arginase from Leishmania (Leishmania) amazonensis and subcellular localization of native enzyme. Mol Biochem Parasitol 159 (2008) 104-111
14. Heby O., Roberts S.C., and Ullman B. Polyamine biosynthetic enzymes as drug targets in parasitic protozoa. Biochem Soc Trans 31 (2003) 415-419
15. Oza S.L., Shaw M.P., Wyllie S., and Fairlamb A.H. Trypanothione biosynthesis in Leishmania major. Mol Biochem Parasitol 139 (2005) 107-116
16. Fairlamb A.H., and Cerami A. Metabolism and functions of trypanothione in the Kinetoplastida. Annu Rev Microbiol 46 (1992) 695-729
17. Krauth-Siegel L.R., Comini M.A., and Schlecker T. The trypanothione system. Subcell Biochem 44 (2007) 231-251
18. Gaur U., Roberts S.C., Dalvi R.P., Corraliza I., Ullman B., and Wilson M.E. An effect of parasite-encoded arginase on the outcome of murine cutaneous leishmaniasis. J Immunol 179 (2007) 8446-8453
19. Castro R., Scott K., Jordan T., et al. The ultrastructure of the parasitophorous vacuole formed by Leishmania major. J Parasitol 92 (2006) 1162-1170
20. Colmenares M., Kar S., Goldsmith-Pestana K., and McMahon-Pratt D. Mechanisms of pathogenesis: differences amongst Leishmania species. Trans R Soc Trop Med Hyg 96 Suppl. 1 (2002) S3-S7
21. Turco S.J., Späth G.F., and Beverley S.M. Is lipophosphoglycan a virulence factor? A surprising diversity between Leishmania species. Trends Parasitol 17 (2001) 223-226
22. Ha D.S., Schwarz J.K., Turco S.J., and Beverley S.M. Use of the green fluorescent protein as a marker in transfected Leishmania. Mol Biochem Parasitol 77 (1996) 57-64
23. Sambrook J., and Russell D.W. Molecular cloning: a laboratory manual. 3rd ed. (2001), Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY
24. Robinson K.A., and Beverley S.M. Improvements in transfection efficiency and tests of RNA interference (RNAi) approaches in the protozoan parasite Leishmania. Mol Biochem Parasitol 128 (2003) 217-228
25. Corraliza I.M., Campo M.L., Soler G., and Modolell M. Determination of arginase activity in macrophages: a micromethod. J Immunol Methods 174 (1994) 231-235
26. Balana-Fouce R., Escribano M.I., and Alunda J.M. Leishmania infantum: polyamine biosynthesis and levels during the growth of promastigotes. Int J Biochem 23 (1991) 1213-1217
27. Cohen S.A., and Michaud D.P. Synthesis of a fluorescent derivatizing reagent, 6-aminoquinolyl-N-hydroxysuccinimidyl carbamate, and its application for the analysis of hydrolysate amino acids via high-performance liquid chromatography. Anal Biochem 211 (1993) 279-287
28. Ruiz-Capillas C., and Moral A. Free amino acids and biogenic amines in red and white muscle of tuna stored in controlled atmospheres. Amino Acids 26 (2004) 125-132
29. Titus R.G., Muller I., Kimsey P., et al. Exacerbation of experimental murine cutaneous leishmaniasis with CD4+ Leishmania major-specific T cell lines or clones which secrete interferon-gamma and mediate parasite-specific delayed-type hypersensitivity. Eur J Immunol 21 (1991) 559-567
30. Zufferey R., Allen S., Barron T., et al. Ether phospholipids and glycosylinositolphospholipids are not required for amastigote virulence or for inhibition of macrophage activation by Leishmania major. J Biol Chem 278 (2003) 44708-44718
31. Shen S., Arhin G.K., Ullu E., and Tschudi C. In vivo epitope tagging of Trypanosoma brucei genes using a one step PCR-based strategy. Mol Biochem Parasitol 113 (2001) 171-173
32. Heby O., Persson L., and Rentala M. Targeting the polyamine biosynthetic enzymes: a promising approach to therapy of African sleeping sickness, Chagas' disease, and leishmaniasis. Amino Acids 33 (2007) 359-366
33. Sacks D.L., and Perkins P.V. Identification of an infective stage of Leishmania promastigotes. Science 223 (1984) 1417-1419
34. Belkaid Y., Mendez S., Lira R., Kadambi N., Milon G., and Sacks D. A natural model of Leishmania major infection reveals a prolonged "silent" phase of parasite amplification in the skin before the onset of lesion formation and immunity. J Immunol 165 (2000) 969-977
35. Papadopoulou B., and Dumas C. Parameters controlling the rate of gene targeting frequency in the protozoan parasite Leishmania. Nucleic Acids Res 25 (1997) 4278-4286
36. Carrillo C., Cejas S., Huber A., Gonzalez N.S., and Algranati I.D. Lack of arginine decarboxylase in Trypanosoma cruzi epimastigotes. J Eukaryot Microbiol 50 (2003) 312-316
37. Ariyanayagam M.R., Tetaud E., and Fairlamb A.H. Diamine auxotrophy in a eukaryotic parasite. Biochem Soc Trans 26 (1998) 606-609
38. Ariyanayagam M.R., and Fairlamb A.H. Diamine auxotrophy may be a universal feature of Trypanosoma cruzi epimastigotes. Mol Biochem Parasitol 84 (1997) 111-121
39. Muller S., Liebau E., Walter R.D., and Krauth-Siegel R.L. Thiol-based redox metabolism of protozoan parasites. Trends Parasitol 20 (2003) 320-328
40. Sakata K., Kashiwagi K., Sharmin S., et al. Increase in putrescine, amine oxidase, and acrolein in plasma of renal failure patients. Biochem Biophys Res Commun 305 (2003) 143-149
41. Shaked-Mishan P., Suter-Grotemeyer M., Yoel-Almagor T., Holland N., Zilberstein D., and Rentsch D. A novel high-affinity arginine transporter from the human parasitic protozoan Leishmania donovani. Mol Microbiol 60 (2006) 30-38
42. Hasne M.P., and Ullman B. Identification and characterization of a polyamine permease from the protozoan parasite Leishmania major. J Biol Chem 280 (2005) 15188-15194
43. Basselin M., Coombs G.H., and Barrett M.P. Putrescine and spermidine transport in Leishmania. Mol Biochem Parasitol 109 (2000) 37-46
44. Kandpal M., and Tekwani B.L. Polyamine transport systems of Leishmania donovani promastigotes. Life Sci 60 (1997) 1793-1801
45. Iniesta V., Carcelen J., Molano I., et al. Arginase I induction during Leishmania major infection mediates the development of disease. Infect Immun 73 (2005) 6085-6090
46. Vincendeau P., Gobert A.P., Daulouede S., Moynet D., and Mossalayi M.D. Arginases in parasitic diseases. Trends Parasitol 19 (2003) 9-12
47. Muleme HM, Reguera RM, Berard A, et al. Infection with arginase deficient Leishmania major reveals a parasite number-dependent and cytokine-independent regulation of host cellular arginase activity and disease pathogenesis. J Immunol 2009, in press.