Inactivation of parasite cysteine proteinases by the NO-donor 4-(phenylsulfonyl)-3-((2-(dimethylamino)ethyl)thio)-furoxan oxalate

Biochimica et Biophysica Acta - Proteins and Proteomics

Volumn 1703, Issue 1, 2004, Pages 69-77

  Ascenzi, Paolo ^a,b   Bocedi, Alessio ^a,b,c   Gentile, Marco ^b   Visca, Paolo ^a,b   Gradoni, Luigi ^d  

^a ROMA TRE UNIVERSITY   (Italy)

^b NATIONAL INSTITUTE FOR INFECTIOUS DISEASES L SPALLANZANI   (Italy)

^c UNIVERSITY OF L'AQUILA   (Italy)

^d ISTITUTO SUPERIORE DI SANITÀ   (Italy)

Author keywords

4 (Phenylsulfonyl) 3 ((2 (dimethylamino)ethyl)thio) furoxan oxalate; Cruzipain; Falcipain; Leishmania infantum cysteine proteinase; NO donor; Parasite cysteine proteinase inactivation

Indexed keywords

4 (PHENYLSULFONYL) 3 [[2 (DIMETHYLAMINO)ETHYL]THIO]FUROXAN OXALATE; ASCORBIC ACID; BENZENE DERIVATIVE; COUMARIN DERIVATIVE; CRUZIPAIN; CYSTEINE PROTEINASE; DITHIOTHREITOL; ENZYME; FALCIPAIN; N ALPHA BENZYLOXYCARBONYLPHENYLARGINYL(7 AMINO 4 METHYLCOUMARIN); NITRIC OXIDE DONOR; UNCLASSIFIED DRUG;

ABSORPTION SPECTROSCOPY; ARTICLE; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; ENZYME INACTIVATION; ENZYME INHIBITION; KINETICS; NITROSYLATION; NONHUMAN; PARASITE; PRIORITY JOURNAL;

ANIMALS; ASCORBIC ACID; CYSTEINE ENDOPEPTIDASES; CYSTEINE PROTEINASE INHIBITORS; DITHIOTHREITOL; DOSE-RESPONSE RELATIONSHIP, DRUG; GLUTATHIONE; HYDROGEN-ION CONCENTRATION; KINETICS; LEISHMANIA INFANTUM; MODELS, MOLECULAR; MOLECULAR STRUCTURE; NITRIC OXIDE; NITRIC OXIDE DONORS; OXADIAZOLES; PARASITES; PLASMODIUM FALCIPARUM; SPECTROPHOTOMETRY; SUBSTRATE SPECIFICITY; TRYPANOSOMA CRUZI;

LEISHMANIA INFANTUM; TRYPANOSOMA;

EID: 9644282926     PISSN: 15709639     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbapap.2004.09.027     Document Type: Article

References (61)

1. P.J. Rosenthal, J.H. McKerrow, D. Rasnick, and J.H. Leech Plasmodium falciparum: inhibitors of lysosomal cysteine proteinases inhibit a trophozoite proteinase and block parasite development Mol. Biochem. Parasitol. 35 1989 177 184
2. S.E. Francis, I.Y. Gluzman, A. Oksman, D. Banerjee, and D.E. Goldberg Characterization of native falcipain, an enzyme involved in Plasmodium falciparum hemoglobin degradation Mol. Biochem. Parasitol. 83 1996 189 200
3. G.H. Coombs, and J.C. Mottram Proteinases of Trypanosomes and Leishmania G. Hide J.C. Mottram G.H. Coombs P.H. Holmes Trypanosomiasis and Leishmaniasis: Biology and Control 1997 CAB International Oxford 177 197
4. P.M. Selzer, X. Chen, V.J. Chan, M. Cheng, G.L. Kenyon, I.D. Kuntz, J.A. Sakanari, F.E. Cohen, and J.H. McKerrow Leishmania major: molecular modeling of cysteine proteases and prediction of new nonpeptide inhibitors Exp. Parasitol. 87 1997 212 221
5. J.C. Mottram, D.R. Brooks, and G.H. Coombs Roles of cysteine proteinases of trypanosomes and Leishmania in host-parasite interactions Curr. Opin. Microbiol. 1 1998 455 460
6. K.A. Scheidt, W.R. Roush, J.H. McKerrow, P.M. Selzer, E. Hansell, and P.J. Rosenthal Structure-based design, synthesis and evaluation of conformationally constrained cysteine protease inhibitors Bioorg. Med. Chem. 6 1998 2477 2494
7. J.H. McKerrow Development of cysteine protease inhibitors as chemotherapy for parasitic diseases: insights on safety, target validation, and mechanism of action Int. J. Parasitol. 29 1999 833 837
8. J.J. Cazzulo Proteinases of Trypanosoma cruzi: potential targets for the chemotherapy of Chagas disease Curr. Top. Med. Chem. 2 2002 1261 1271
9. F. Lecaille, J. Kaleta, and D. Gromme Human and parasitic papain-like cysteine proteases: their role in physiology and pathology and recent developments in inhibitor design Chem. Rev. 102 2002 4459 4488
10. P.J. Rosenthal Hydrolysis of erythrocyte proteins by proteases of malaria parasites Curr. Opin. Hematol. 9 2002 140 145
11. A.J. Barrett N.D. Rawlings J.F. Woessner Handbook of Proteolytic Enzymes 2nd ed. 2004 Academic Press London
12. G. Venturini, M. Colasanti, L. Salvati, L. Gradoni, and P. Ascenzi Nitric oxide inhibits falcipain, the Plasmodium falciparum trophozoite cysteine protease Biochem. Biophys. Res. Commun. 267 2000 190 193
13. G. Venturini, L. Salvati, M. Muolo, M. Colasanti, L. Gradoni, and P. Ascenzi Nitric oxide inhibits cruzipain, the major papain-like cysteine proteinase from Trypanosoma cruzi Biochem. Biophys. Res. Commun. 270 2000 437 441
14. P. Ascenzi, L. Salvati, M. Bolognesi, M. Colasanti, F. Polticelli, and G. Venturini Inhibition of cysteine protease activity by NO-donors Curr. Protein Pept. Sci. 2 2001 137 153
15. M. Colasanti, L. Salvati, G. Venturini, P. Ascenzi, and L. Gradoni Cysteine protease as a target for nitric oxide in parasitic organisms Trends Parasitol. 17 2001 575
16. L. Salvati, M. Mattu, M. Colasanti, S. Scalone, G. Venturini, L. Gradoni, and P. Ascenzi NO donors inhibit Leishmania infantum cysteine proteinase activity Biochim. Biophys. Acta 1545 2001 357 366
17. A. Bocedi, L. Gradoni, E. Menegatti, and P. Ascenzi Kinetics of parasite cysteine proteinase inactivation by NO-donors Biochem. Biophys. Res. Commun. 315 2004 710 718
18. K.A. Rockett, M.M. Awburn, W.B. Cowden, and I.A. Clark Killing of Plasmodium falciparum in vitro by nitric oxide derivatives Infect. Immun. 59 1991 3280 3283
19. G.N.R. Vespa, F.Q. Cunha, and J.S. Silva Nitric oxide is involved in control of Trypanosoma cruzi-induced parasitemia and directly kills the parasite in vitro Infect. Immun. 62 1994 5177 5182
20. P. Petray, E. Castanos-Velez, S. Grinstein, A. Örn, and M.E. Rottenberg Role of nitric oxide in resistance and histopathology during experimental infection with Trypanosoma cruzi Immun. Lett. 47 1995 121 126
21. A.P. Gobert, S. Semballa, S. Daulouede, S. Lesthelle, M. Taxile, B. Veyret, and P. Vincendeau Murine macrophages use oxygen- and nitric oxide-dependent mechanisms to synthesize S-nitroso-albumin and to kill extracellular trypanosomes Infect. Immun. 66 1998 4068 4072
22. B. Zeina, C. Banfield, and S. al-Assad Topical glyceryl trinitrate: a possible treatment for cutaneous leishmaniasis Clin. Exp. Dermatol. 22 1997 244 245
23. P. Lopez-Jaramillo, C. Ruano, J. Rivera, E. Teran, R. Salazar-Irigoyen, J.V. Esplugues, and S. Moncada Treatment of cutaneous leishmaniasis with nitric-oxide donor Lancet 351 1998 1176 1177
24. R.N. Davidson, V. Yardley, S.L. Croft, P. Konecny, and N. Benjamin A topical nitric oxide-generating therapy for cutaneous leishmaniasis Trans. R. Soc. Trop. Med. Hyg. 94 2000 319 322
25. G. Sorba, C. Medana, R. Fruttero, C. Cena, A. Di Stilo, U. Galli, and A. Gasco Water soluble furoxan derivatives as NO prodrugs J. Med. Chem. 40 1997 463 469
26. T. Persichini, M. Colasanti, M. Fraziano, V. Coalizzi, C. Medana, F. Polticelli, G. Venturini, and P. Ascenzi Nitric oxide inhibits the HIV-1 reverse transcriptase activity Biochem. Biophys. Res. Commun. 258 1999 624 627
27. 1-antagonist and NO-like vasodilator activities J. Med. Chem. 38 1995 4944 4949
28. D. Boschi, A. Di Stilo, C. Cena, M. Lolli, R. Fruttero, and A. Gasco Studies on agents with mixed NO-dependent vasodilator and β-blocking activities Pharm. Res. 14 1997 1750 1758
29. A. Di Stilo, S. Visentin, C. Cena, M.A. Gasco, G. Ermondi, and A. Gasco New 1,4-dihydropyridines conjugated to furoxanyl moieties, endowed with both nitric oxide-like and calcium channel antagonist vasodilator activities J. Med. Chem. 41 1998 5393 5401
30. 2-antagonists containing NO-donor moieties, endowed with mixed antisecretory and gastroprotective activities Helv. Chim. Acta 83 2000 287 299
31. G. Coruzzi, M. Adami, G. Morini, C. Pozzoli, C. Cena, M. Bertinaria, and A. Gasco Antisecretory and gastroprotective activities of compounds endowed with H2 antagonistic and nitric oxide (NO) donor properties J. Physiol. (Paris) 94 2000 5 10
32. C. Cena, S. Visentin, A. Di Stilo, D. Boschi, R. Fruttero, and A. Gasco Studies on agents with mixed NO-dependent and calcium channel antagonistic vasodilating activities Pharm. Res. 18 2001 157 165
33. M.L. Lolli, C. Cena, C. Medana, L. Lazzarato, G. Morini, G. Coruzzi, S. Manarini, R. Fruttero, and A. Gasco A new class of ibuprofen derivatives with reduced gastrotoxicity J. Med. Chem. 44 2001 3463 3468
34. C. Cena, S. Visentin, A. Gasco, P.A. Martorana, R. Fruttero, and A. Gasco Platelet antiaggregatory effects and haemodynamic activity of two terfuroxan isomer pairs Il Farmaco 57 2002 417 420
35. 3-antagonists endowed with NO-donor properties Bioorg. Med. Chem. 11 2003 1197 1205
36. C. Cena, M.L. Lolli, L. Lazzarato, E. Guaita, G. Morini, G. Coruzzi, S.P. McElroy, I.L. Megson, R. Fruttero, and A. Gasco Antiinflammatory, gastrosparing, and antiplatelet properties of new NO-donor esters of aspirin J. Med. Chem. 46 2003 747 754
37. 1- antagonists J. Med. Chem. 46 2003 3762 3765
38. G. Sorba, U. Galli, C. Cena, R. Fruttero, A. Gasco, G. Morini, M. Adami, G. Coruzzi, M.I. Brenciaglia, and F. Dubini A new furoxan NO-donor rabeprazole derivative and related compounds ChemBioChem 4 2003 899 903
39. A.P.C.A. Lima, J. Scharfstein, A.C. Storer, and R. Ménard Temperature-dependent substrate inhibition of the cysteine proteinase (GP57/51) from Trypanosoma cruzi Mol. Biochem. Parasitol. 56 1992 335 338
40. C. Labriola, M. Sousa, and J.J. Cazzulo Purification of the major cysteine proteinase (cruzipain) from Trypanosoma cruzi by affinity chromatography Biol. Res. 26 1993 101 107
41. V. Stoka, M. Nycander, B. Lenarcic, C. Labriola, J.J. Cazzulo, I. Bjork, and V. Turk Inhibition of cruzipain, the major cysteine proteinase of the protozoan parasite, Trypanosoma cruzi, by proteinase inhibitors of the cystatin superfamily FEBS Lett. 370 1995 101 104
42. L. Salvati, M. Mattu, F. Polticelli, F. Tiberi, L. Gradoni, G. Venturini, M. Bolognesi, and P. Ascenzi Modulation of the catalytic activity of cruzipain, the major cysteine proteinase from Trypanosoma cruzi, by temperature and pH Eur. J. Biochem. 268 2001 3253 3258
43. E. Antonini, and M. Brunori Hemoglobin and Myoglobin in their Reactions with Ligands 1971 North Holland Publishing Amsterdam
44. M. Feelisch, D. Kubitzek, and J. Werringgloer The oxyhemoglobin assay M. Feelisch J.S. Stamler Methods in Nitric Oxide Research 1996 Wiley Chichester 455 478
45. M. Xian, X. Chen, Z. Liu, K. Wang, and P.G. Wang Inhibition of papain by S-nitrosothiols: formation of mixed disulfides J. Biol. Chem. 275 2000 20467 20473
46. J. Wyman Linked functions and reciprocal effects in hemoglobin: a second look Adv. Protein Chem. 19 1964 223 286
47. P. Ascenzi, E. Menegatti, and G. Amiconi pH effects in biochemical reactions: what's the meaning of pK and midpoint? Biochem. Educ. 16 1988 93 94
48. L. Polgár, and P. Halasz Current problems in mechanistic studies of serine and cysteine proteinases Biochem. J. 207 1982 1 10
49. V. Stoka, J.H. McKerrow, J.J. Cazzulo, and V. Turk Substrate inhibition of cruzipain is not affected by the C-terminal domain FEBS Lett. 429 1998 129 133
50. M.E. McGrath, A.E. Eakin, J.C. Engel, J.H. McKerrow, C.S. Craik, and R.J. Fletterick The crystal structure of cruzain: a therapeutic target for Chagas' disease J. Mol. Biol. 247 1995 251 259
51. S.A. Gillmor, C.S. Craik, and R.J. Fletterick Structural determinants of specificity in the cysteine protease cruzain Protein Sci. 6 1997 1603 1611
52. D.L.H. Williams The chemistry of S-nitrosothiols Acc. Chem. Res. 32 1999 869 876
53. H.M. Berman, J. Westbrook, Z. Feng, G. Gilliland, T.N. Bhat, H. Weissig, I. Shindyalov, and P.E. Bourne The protein data bank Nucleic Acids Res. 28 2000 235 242
54. B. Boeckmann, A. Bairoch, R. Apweiler, M.-C. Blatter, A. Estreicher, E. Gasteiger, M.J. Martin, K. Michoud, C. O'Donovan, I. Phan, S. Pilbout, and M. Schneider The SWISS-PROT protein knowledgebase and its supplement TrEMBL in 2003 Nucleic Acids Res. 31 2003 365 370
55. J.S. Stamler Redox signaling: nitrosylation and related target interactions of nitric oxide Cell 78 1994 931 936
56. C.E. Cooper Nitric Oxide Biochemistry Biochim. Biophys. Acta vol. 1411 1999
57. W. Cao, M.L. Baniecki, W.J. McGrath, C. Bao, C.B. Deming, J.J. Rade, C.J. Lowenstein, and W.F. Mangel Nitric oxide inhibits the adenovirus proteinase in vitro and viral infectivity in vivo FASEB J. 17 2003 2345 2346
58. A. Sannella, L. Gradoni, T. Persichini, E. Ongini, G. Venturini, and M. Colasanti Intracellular release of nitric oxide by NCX 972, an NO-releasing metronidazole, enhances in vitro killing of Entamoeba histolytica Antimicrob. Agents Chemother. 47 2003 2303 2306
59. R. Siman-Tov, and S. Ankri Nitric oxide inhibits cysteine proteinases and alcohol dehydrogenase 2 of Entamoeba histolytica Parasitol. Res. 89 2003 146 149
60. H.A. Sober Handbook of Biochemistry-Selected Data for Molecular Biology 1968 The Chemical Rubber Cleveland 186
61. R. Koradi, M. Billeter, and K. Wuthrich MOLMOL: a program for display and analysis of macromolecular structures J. Mol. Graph. 14 1996 51 55