Inhibition profile of Leishmania mexicana arginase reveals differences with human arginase I

International Journal for Parasitology

Volumn 41, Issue 5, 2011, Pages 545-552

  Riley, Eric ^a   Roberts, Sigrid C ^b   Ullman, Buddy ^a  

^a OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^b PACIFIC UNIVERSITY   (United States)

Author keywords

Amino acids; Arginase; Inhibitors; Leishmania; Polyamines

Indexed keywords

ARGINASE; ARGINASE 1; ARGININE; DIVALENT CATION; ENZYME INHIBITOR; MANGANESE; RECOMBINANT ARGINASE; RECOMBINANT ARGINASE 1; UNCLASSIFIED DRUG;

AMINO ACID; COLIFORM BACTERIUM; DEFENSE MECHANISM; ENZYME; EUKARYOTE; INHIBITION; INHIBITOR; PARASITE; PH; PROTOZOAN; UREA;

ARTICLE; CONTROLLED STUDY; ENZYME INHIBITION; ENZYME KINETICS; ENZYME PURIFICATION; ENZYME SPECIFICITY; ESCHERICHIA COLI; LEISHMANIA MEXICANA; NONHUMAN; NUCLEOTIDE SEQUENCE; PH;

ANIMALS; ARGINASE; DOWN-REGULATION; ENZYME INHIBITORS; HUMANS; KINETICS; LEISHMANIA MEXICANA; LEISHMANIASIS, CUTANEOUS; MICE; PROTOZOAN PROTEINS;

ESCHERICHIA COLI; EUKARYOTA; LEISHMANIA MEXICANA;

EID: 79952695042     PISSN: 00207519     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ijpara.2010.12.006     Document Type: Article

References (33)

1. Ash D.E. Structure and function of arginases. J. Nutr. 2004, 134:2760S-2764S.
2. Ash D.E., Cox J.D., Christianson D.W. Arginase: a binuclear manganese metalloenzyme. Met. Ions Biol. Syst. 2000, 37:407-428.
3. Beruter J., Colombo J.P., Bachmann C. Purification and properties of arginase from human liver and erythrocytes. Biochem. J. 1978, 175:449-454.
4. Cama E., Colleluori D.M., Emig F.A., Shin H., Kim S.W., Kim N.N., Traish A.M., Ash D.E., Christianson D.W. Human arginase II: crystal structure and physiological role in male and female sexual arousal. Biochemistry 2003, 42:8445-8451.
5. Cama E., Emig F.A., Ash D.E., Christianson D.W. Structural and functional importance of first-shell metal ligands in the binuclear manganese cluster of arginase I. Biochemistry 2003, 42:7748-7758.
6. Cama E., Shin H., Christianson D.W. Design of amino acid sulfonamides as transition-state analogue inhibitors of arginase. J. Am. Chem. Soc. 2003, 125:13052-13057.
7. Cox J.D., Cama E., Colleluori D.M., Pethe S., Boucher J.L., Mansuy D., Ash D.E., Christianson D.W. Mechanistic and metabolic inferences from the binding of substrate analogues and products to arginase. Biochemistry 2001, 40:2689-2701.
8. da Silva E.R., da Silva M.F., Fischer H., Mortara R.A., Mayer M.G., Framesqui K., Silber A.M., Floeter-Winter L.M. Biochemical and biophysical properties of a highly active recombinant arginase from Leishmania (Leishmania) amazonensis and subcellular localization of native enzyme. Mol. Biochem. Parasitol. 2008, 159:104-111.
9. Darlyuk I., Goldman A., Roberts S.C., Ullman B., Rentsch D., Zilberstein D. Arginine homeostasis and transport in the human pathogen Leishmania donovani. J. Biol. Chem. 2009, 284:19800-19807.
10. Di Costanzo L., Ilies M., Thorn K.J., Christianson D.W. Inhibition of human arginase I by substrate and product analogues. Arch. Biochem. Biophys. 2010, 496:101-108.
11. Di Costanzo L., Moulin M., Haertlein M., Meilleur F., Christianson D.W. Expression, purification, assay, and crystal structure of perdeuterated human arginase I. Arch. Biochem. Biophys. 2007, 465:82-89.
12. Di Costanzo L., Sabio G., Mora A., Rodriguez P.C., Ochoa A.C., Centeno F., Christianson D.W. Crystal structure of human arginase I at 1.29-A resolution and exploration of inhibition in the immune response. Proc. Natl. Acad. Sci. USA 2005, 102:13058-13063.
13. El Kasmi K.C., Qualls J.E., Pesce J.T., Smith A.M., Thompson R.W., Henao-Tamayo M., Basaraba R.J., Konig T., Schleicher U., Koo M.S., Kaplan G., Fitzgerald K.A., Tuomanen E.I., Orme I.M., Kanneganti T.D., Bogdan C., Wynn T.A., Murray P.J. Toll-like receptor-induced arginase 1 in macrophages thwarts effective immunity against intracellular pathogens. Nat. Immunol. 2008, 9:1399-1406.
14. Gaur U., Roberts S.C., Dalvi R.P., Corraliza I., Ullman B., Wilson M.E. An effect of parasite-encoded arginase on the outcome of murine cutaneous leishmaniasis. J. Immunol. 2007, 179:8446-8453.
15. Iniesta V., Carcelen J., Molano I., Peixoto P.M., Redondo E., Parra P., Mangas M., Monroy I., Campo M.L., Nieto C.G., Corraliza I. Arginase I induction during Leishmania major infection mediates the development of disease. Infect. Immun. 2005, 73:6085-6090.
16. Iniesta V., Gomez-Nieto L.C., Corraliza I. The inhibition of arginase by N(omega)-hydroxy-l-arginine controls the growth of Leishmania inside macrophages. J. Exp. Med. 2001, 193:777-784.
17. Iniesta V., Gomez-Nieto L.C., Molano I., Mohedano A., Carcelen J., Miron C., Alonso C., Corraliza I. Arginase I induction in macrophages, triggered by Th2-type cytokines, supports the growth of intracellular Leishmania parasites. Parasite Immunol. 2002, 24:113-118.
18. Iovannisci D.M., Ullman B. High efficiency plating method for Leishmania promastigotes in semidefined or completely-defined medium. J. Parasitol. 1983, 69:633-636.
19. Kropf P., Fuentes J.M., Fahnrich E., Arpa L., Herath S., Weber V., Soler G., Celada A., Modolell M., Muller I. Arginase and polyamine synthesis are key factors in the regulation of experimental leishmaniasis in vivo. FASEB J. 2005, 19:1000-1002.
20. Kropf P., Herath S., Weber V., Modolell M., Muller I. Factors influencing Leishmania major infection in IL-4-deficient Balb/c mice. Parasite Immunol. 2003, 25:439-447.
21. Louis C.A., Mody V., Henry W.L., Reichner J.S., Albina J.E. Regulation of arginase isoforms I and II by IL-4 in cultured murine peritoneal macrophages. Am. J. Physiol. 1999, 276:R237-242.
22. Mauel J., Ransijn A., Buchmuller-Rouiller Y. Killing of Leishmania parasites in activated murine macrophages is based on an l-arginine-dependent process that produces nitrogen derivatives. J. Leukoc. Biol. 1991, 49:73-82.
23. Muleme H.M., Reguera R.M., Berard A., Azinwi R., Jia P., Okwor I.B., Beverley S., Uzonna J.E. 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, 183:8068-8076.
24. Munder M., Eichmann K., Moran J.M., Centeno F., Soler G., Modolell M. Th1/Th2-regulated expression of arginase isoforms in murine macrophages and dendritic cells. J. Immunol. 1999, 163:3771-3777.
25. Pegg A.E. Mammalian polyamine metabolism and function. IUBMB Life 2009, 61:880-894.
26. Pegg A.E., McCann P.P. Polyamine metabolism and function. Am. J. Physiol. 1982, 243:C212-221.
27. Reguera R.M., Balana-Fouce R., Showalter M., Hickerson S., Beverley S.M. Leishmania major lacking arginase (ARG) are auxotrophic for polyamines but retain infectivity to susceptible BALB/c mice. Mol. Biochem. Parasitol. 2009, 165:48-56.
28. Roberts S.C., Tancer M.J., Polinsky M.R., Gibson K.M., Heby O., Ullman B. Arginase plays a pivotal role in polyamine precursor metabolism in Leishmania. Characterization of gene deletion mutants. J. Biol. Chem. 2004, 279:23668-23678.
29. Sastre M., Galea E., Feinstein D., Reis D.J., Regunathan S. Metabolism of agmatine in macrophages: modulation by lipopolysaccharide and inhibitory cytokines. Biochem. J. 1998, 330(Pt 3):1405-1409.
30. Segel I. Enzyme Kinetics; Behaviour and Analysis of Rapid Equilibrium and Steady State Enzyme Systems 1975, Wiley, John and Sons, New York.
31. Shin H., Cama E., Christianson D.W. Design of amino acid aldehydes as transition-state analogue inhibitors of arginase. J. Am. Chem. Soc. 2004, 126:10278-10284.
32. Taylor-Robinson A. Th1/Th2-regulated arginase availability modulates Leishmania infection. Trends Parasitol. 2001, 17:262.
33. Wanasen N., Soong L. l-arginine metabolism and its impact on host immunity against Leishmania infection. Immunol. Res. 2008, 41:15-25.