Heparin modulates the endopeptidase activity of Leishmania mexicana cysteine protease cathepsin L-like rCPB2.8

PLoS ONE

Volumn 8, Issue 11, 2013, Pages

  Judice, Wagner A S ^a   Manfredi, Marcella A ^a   Souza, Gerson P ^a   Sansevero, Thiago M ^a   Almeida, Paulo C ^b   Shida, Cláudio S ^b   Gesteira, Tarsis F ^c   Juliano, Luiz ^b   Westrop, Gareth D ^d   Sanderson, Sanya J ^d   Coombs, Graham H ^d   Tersariol, Ivarne L S ^a,b  

^a UNIVERSIDADE DE MOGI DAS CRUZES   (Brazil)

^b FEDERAL UNIVERSITY OF SÃO PAULO   (Brazil)

^c CINCINNATI CHILDREN'S HOSPITAL MEDICAL CENTER   (United States)

^d UNIVERSITY OF STRATHCLYDE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMALS; BASE SEQUENCE; CATHEPSIN L; CIRCULAR DICHROISM; CLONING, MOLECULAR; DNA PRIMERS; HEPARIN; KINETICS; LEISHMANIA MEXICANA; POLYMERASE CHAIN REACTION; SPECTROMETRY, FLUORESCENCE;

EID: 84894313105     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0080153     Document Type: Article

References (71)

1. Sajid M, McKerrow JH (2002) Cysteine proteases of parasitic organisms. Mol Biochem Parasitol 120: 1-21. Review. Erratum in: Mol Biochem Parasitol 121: 159.
2. Coombs GH (1982) Proteinases of Leishmania mexicana and other flagellate protozoa. Parasitology 84: 149-155.
3. Pupkis MF, Coombs GH (1984) Purification and characterization of proteolytic enzymes of Leishmania mexicana amastigotes and promastigotes. J Gen Microbiol 130: 2375-2383.
4. Robertson CD, Coombs GH (1990) Characterization of three groups of cysteine proteinases in the amastigotes of Leishmania mexicana mexicana. Mol Biochem Parasitol 42: 269-276.
5. Robertson CD, Coombs GH (1992) Stage-specific proteinases of Leishmania mexicana promastigotes. FEMS Microbiol Lett 94: 127-132.
6. Bates PA, Robertson CD, Coombs GH (1994) Expression of cysteine proteinases by metacyclic promastigotes of Leishmania mexicana. J Euk Microbiol 41: 199-203.
7. Mottram JC, Frame MC, Brooks DR, Tetley L, Hutchison JE, et al. (1997) The multiple cpb cysteine proteinase genes of Leishmania mexicana encode isoenzymes that differ in their stage regulation and substrate preferences. J Biol Chem 272: 14285-14293.
8. Souza AE, Waugh S, Coombs GH, Mottram JC (1992) Characterization of a multicopy gene for a major stage-specific cysteine proteinase of Leishmania mexicana. FEBS Lett 311: 124-127.
9. Robertson CD, Coombs GH (1994) Multiple high activity cysteine proteases of Leishmania mexicana are encoded by the lmcpb gene array. Microbiology 140: 417-424.
10. Mottram JC, Souza AE, Hutchison JE, Carter R, Frame MJ, et al. (1996). Evidence from disruption of the lmcpb gene array of Leishmania mexicana that cysteine proteinases are virulence factors. Proc Natl Acad Sci USA 93: 6008-6013.
11. Coombs GH, Mottram JC (1997) Proteinases of trypanosomes and Leishmania. In: Hide, G, Mottram, JC, Coombs, GH, Holmes, PH, editors. Trypanosomiasis and leishmaniasis: biology and control. Oxford: Oxford-CAB International. pp. 177-197.
12. Traub-Cseko YM, Duboise M, Boukai LK, McMahon-Pratt D (1993) Identification of two distinct cysteine proteinase genes of Leishmania pifanoi axenic amastigotes using the polymerase chain reaction. Mol Biochem Parasitol 57: 101-116.
13. Sakanari JA, Nadler SA, Chan VJ, Engel JC, Leptak C, et al. (1997) Leishmania major: comparison of the cathepsin L- and B-like cysteine protease genes with those of other trypanosomatids. Exp Parasitol 85: 63-76.
14. Campetella O, Henriksson J, Åslund L, Frasch ACC, Pettersson U, et al. (1992) The major cysteine proteinase (cruzipain) from Trypanosoma cruzi is encoded by multiple polymorphic tandemly organized genes located on different chromosomes. Mol Biochem Parasitol 50: 225-234.
15. Murta ACM, Persechini PM, Padron TS, Souza W, Guimarães JA, et al. (1990) Structural and functional identification of GP57/51 antigen of Trypanosoma cruzi as a cysteine proteinase. Mol Biochem Parasitol 43: 27-38.
16. Mottram JC, North MJ, Barry JD, Coombs GH (1989) A cysteine proteinase cDNA from Trypanosoma brucei predicts an enzyme with an unusual C-terminal extension. FEBS Lett 258: 211-215.
17. Coombs GH, Mottram JC (1997) Parasite Proteinases and Amino Acid Metabolism: Possibilities for Chemotherapeutic Exploitation. Parasitology 114: S61-S80.
18. DeSouza LS, Lang T, Prina E, Hellio R, Antoine JC (1995) Intracellular Leishmania amazonensis Amastigotes Internalize and Degrade MHC Class II Molecules of Their Host Cells. J Cell Sci 108: 3219-3231.
19. Alexander J, Coombs GH, Mottram JC (1998) Leishmania mexicana Cysteine Proteinase- Deficient Mutants Have Attenuated Virulence for Mice and Potentiate a Th1 Response. J Immunol161: 6794-6801.
20. Barrett MP, Mottram JC, Coombs GH (1999) Recent advances in identifying and validating drug targets in trypanosomes and leishmanias. Trends Microbiol 7: 82-88.
21. Caffrey CR, Scory S, Steverding D (2000) Cysteine proteinases of trypanosome parasites: novel targets for chemotherapy. Curr Drug Targets 1: 155-162.
22. Sanderson SJ, Pollock KG, Hilley JD, Meldal M, St Hilaire PM, et al. (2000) Expression and characterization of a recombinant cysteine proteinase of Leishmania mexicana. Biochem J 347: 383-388.
23. Alves LC, Melo RL, Sanderson SJ, Mottram JC, Coombs GH, et al. (2001) S1 subsite specificity of a recombinant cysteine proteinase, CPB, of Leishmania Mexicana compared with cruzain, human cathepsin L and papain using substrates containing non-natural basic amino acids. Eur J Biochem 268: 1206-1212.
24. Alves LC, Judice WA, St Hilaire PM, Meldal M, Sanderson SJ, et al. (2001) Substrate specificity of recombinant cysteine proteinase, CPB, of Leishmania mexicana. Mol Biochem Parasitol 116: 1-9.
25. Alves LC, Melo RL, Cezari MH, Sanderson SJ, Mottram JC, et al. (2001) Analysis of the S2 subsite specificities of the recombinant cysteine proteinases CPB of Leishmania mexicana, and cruzain of Trypanosoma cruzi, using fluorescent substrates containing non-natural basic amino acids. Mol Biochem Parasitol 117: 137-143.
26. St Hilaire PM, Alves LC, Sanderson SJ, Mottram JC, Juliano MA, et al. (2000) The substrate specificity of a recombinant cysteine protease from Leishmania mexicana: application of a combinatorial peptide library approach. Chem Biol Chem 1: 115-122.
27. Juliano MA, Brooks DR, Selzer PM, Pandolfo HL, Judice WA, et al (2004) Differences in substrate specificities between cysteine protease CPB isoforms of Leishmania mexicana are mediated by a few amino acid changes. Eur J Biochem 271: 3704-3714.
28. Alves LC, St Hilaire PM, Meldal M, Sanderson SJ, Mottram JC, et al. (2001) Identification of peptides inhibitory to recombinant cysteine proteinase, CPB, of Leishmania mexicana. Mol Biochem Parasitol 114: 81-88.
29. St Hilaire PM, Alves LC, Herrera F, Renil M, Sanderson S, et al (2002) Solid-Phase library synthesis, screening and selection of tight-binding reduced peptide bond inhibitors of a recombinant Leishmania mexicana cysteine protease B. J Med Chem 45: 1971-1982.
30. Graven A, St Hilaire PM, Sanderson SJ, Mottram JC, Coombs GH, et al. (2001) Combinatorial library of peptide isosters based on Diels-Alder reactions: identification of novel inhibitors against a recombinant cysteine protease from Leishmania mexicana. J Comb Chem 3: 441-452.
31. Stoka V, McKerrow JH, Cazzulo JJ, Turk V (1998) Substrate inhibition of cruzipain is not affected by the C-terminal domain. FEBS Lett 429: 129-133.
32. Conrad HE (1998) Heparin-Binding Proteins. Academic Press Inc., New York.
33. Del Nery E, Juliano MA, Lima APCA, Scharfstein J, Juliano L (1997) Kininogenase activity by the major cysteinyl proteinase (cruzipain) from Trypanosoma cruzi. J Biol Chem 272: 25713-25718.
34. Bartlett AH, Park PW (2010) Proteoglycans in host-pathogen interactions: molecular mechanisms and therapeutic implications. Expert Rev Mol Med 12: e5.
35. Love DC, Esko JD, Mosser DM (1993) A heparin-binding activity on Leishmania amastigotes which mediates adhesion to cellular proteoglycans. J Biol Chem 123: 759-766.
36. de Castro Côrtes LM, de Souza Pereira MC, da Silva FS, Pereira BA, de Oliveira Junior FO, et al. (2012) Participation of heparin binding proteins from the surface of Leishmania (Viannia) braziliensis promastigotes in the adhesion of parasites to Lutzomyia longipalpis cells (Lulo) in vitro. Parasit Vectors 5: 142.
37. Kulkarni MM, Jones EA, McMaster WR, McGwire BS (2008) Fibronectin binding and proteolytic degradation by Leishmania and effects on macrophage activation. Infect Immun 76: 1738-1747
38. Almeida PC, Nantes IL, Rizzi CCA, Judice WAS, Chagas JR, et al. (1999) Cysteine proteinase activity regulation. A possible role of heparin and heparin-like glycosaminoglycans. J Biol Chem 274: 30433-30438.
39. Almeida PC, Nantes IL, Chagas JR, Rizzi CCA, Faljoni-Alário A, et al. (2001) Cathepsin B activity regulation. Heparin-like glycosaminogylcans protect human cathepsin B from alkaline pH-induced inactivation. J Biol Chem 276: 944-951.
40. Lima APCA, Almeida PC, Tersariol ILS, Schmitz V, Schmaier AH, et al. (2002) Heparan sulfate modulates kinin release by Trypanosoma cruzi through the activity of cruzipain. J Biol Chem 277: 5875-5881.
41. Li Z, Hou WS, Bromme D (2000) Collagenolytic activity of cathepsin K is specifically modulated by cartilage-resident chondroitin sulfates. Biochemistry 39: 529-536.
42. Ayala YM, Di Cera E (2000) A simple method for the determination of individual rate constants for substrate hydrolysis by serine proteases. Protein Sci 9: 1589-1593.
43. Judice WA, Cezari MH, Lima AP, Scharfstein J, Chagas JR, et al. (2001) Comparison of the specificity, stability and individual rate constants with respective activation parameters for the peptidase activity of cruzipain and its recombinant form, cruzain, from Trypanosoma cruzi. Eur J Biochem 268: 6578-6586.
44. Judice WA, Mottram JC, Coombs GH, Juliano MA, Juliano L (2005) Specific negative charges in cysteine protease isoforms of Leishmania mexicana are highly influential on the substrate binding and hydrolysis. Mol Biochem Parasitol 144: 36-43.
45. Laidler KJ, Peterman BF (1979) Temperature effects in enzyme kinetics. Methods in Enzymology 63: 234-257.
46. Cornish-Bowden A (1999) Fundaments of Enzyme Kinetics. Portland Press, London, UK.
47. Polgar L (1999) Oligopeptidase B: a new type of serine peptidase with unique substrate-dpendent temperature sensitivity. Biochemistry 38: 15548-15555
48. Pimenta DC, Nantes IL, de Souza ES, Le Bonniec B, Ito AS, et al. (2002) Interaction of heparin with internally quenched fluorogenic peptides derived from heparin-binding consensus sequences, kallistatin and anti-thrombin III. Biochem J 366: 435-446.
49. Shinjo SK, Tersariol IL, Oliveira V, Nakaie CR, Oshiro ME, et al. (2002) Heparin and heparan sulfate disaccharides bind to the exchanger inhibitor peptide region of Na+/Ca2+ exchanger and reduce the cytosolic calcium of smooth muscle cell lines. Requirement of C4-C5 unsaturation and 1 4 glycosidic linkage for activity. J Biol Chem 277: 48227-48233
50. Sreerama N, Woody RW (2004) Computation and Analysis of Protein Circular Dichroism Spectra. Methods in Enzymology 383: 318-351
51. Nägler DK, Storer AC, Portaro FC, Carmona E, Juliano L, et al.(1997) Major increase in endopeptidase activity of human cathepsin B upon removal of occluding loop contacts. Biochemistry 36: 12608-12615.
52. Barrett AJ (1980) Fluorimetric assays for cathepsin B and cathepsin H with methylcoumarylamide substrates. Biochem J 187: 909-912.
53. Nunes GLC, Simões A, Dyszy FH, Shida CS, Juliano MA, et al. (2011) Mechanism of Heparin Acceleration of Tissue Inhibitor of Metalloproteases-1 (TIMP-1) Degradation by the Human Neutrophil Elastase. PLoS One 6: e21525
54. Schneck JL, Villa JP, McDevitt P, McQueney MS, Thrall SH, et al. (2008) Chemical Mechanism of a Cysteine Protease, Cathepsin C, As Revealed by Integration of both Steady-State and Pre-Steady-State Solvent Kinetic Isotope Effects. Biochemistry 47: 8697-8710
55. Stein RL, Strimpler AM, Hori H, Powers JC (1987) Catalysis by human leukocyte elastase. Aminolysis of acyl-enzymes by amino acid amides and peptides. Biochemistry 26: 2238-2242.
56. Xu H, Bush LA, Pineda AO, Caccia S, Di Cera E (2005) Thrombomodulin Changes the Molecular Surface of Interaction and the Rate of Complex Formation between Thrombin and Protein C. J Biol Chem 280: 7956-7961.
57. van Holde KE (2002) A hypothesis concerning diffusion-limited protein-ligand interactions. Biophys Chem 101-102: 249-254.
58. Hussain S, Khan A, Gul S, Resmini M, Verma CS, et al. (2011) Identification of interactions involved in the generation of nucleophilic reactivity and of catalytic competence in the catalytic site Cys/His ion pair of papain. Biochemistry 50: 10732-10742.
59. Hussain S, Pinitglang S, Bailey TS, Reid JD, Noble MA, et al. (2003) Variation in the pH-dependent pre-steady-state and steady-state kinetic characteristics of cysteine-proteinase mechanism: evidence for electrostatic modulation of catalytic-site function by the neighbouring carboxylate anion. Biochem J 372: 735-746.
60. Gesteira TF, Coulson-Thomas VJ, Taunay-Rodrigues A, Oliveira V, Thacker BE, et al. (2011) Inhibitory peptides of the sulfotransferase domain of the heparan sulfate enzyme, N-deacetylase-N-sulfotransferase-1. J Biol Chem 286: 5338-4536.
61. Koti ASR, Krishna MMG, Periasamy N (2001) Time-resolved area-normalized emission spectroscopy (TRANES): a novel method for confirming emission from two excited states, J Phys Chem A 105: 1767-1771.
62. Carmona E, Dufour E, Plouffe C, Takebe S, Mason P, et al. (1996) Potency and selectivity of the cathepsin L propeptide as an inhibitor of cysteine proteases. Biochemistry 35: 8149-8157.
63. Coulombe R, Grochulski P, Sivaraman J, Ménard R, Mort JS, et al. (1996) Structure of human procathepsin L reveals the molecular basis of inhibition by the prosegment. EMBO J 15: 5492-5503.
64. Mason RW, Gal S, Gottesman MM (1987) The identification of the major excreted protein (MEP) from a transformed mouse fibroblast cell line as a catalytically active precursor form of cathepsin L. Biochem J 248: 449-454.
65. Pungercar JR, Caglic D, Sajid M, Dolinar M, Vasiljeva O, et al. (2009) Autocatalytic processing of procathepsin B is triggered by proenzyme activity. FEBS J 276: 660-668.
66. Fairhead M, Kelly SM, van der Walle CF (2008) A heparin binding motif on the pro-domain of human procathepsin L mediates zymogen destabilization and activation. Biochem Biophys Res Commun 366: 862-867.
67. Horn M, Jílková A, Vondrášek J, Marešová L, Caffrey CR, et al. (2011) Mapping the Pro-Peptide of the Schistosoma mansoni Cathepsin B1 Drug Target: Modulation of Inhibition by Heparin and Design of Mimetic Inhibitors. ACS Chem Biol 6: 609-617.
68. Caglic D, Pungercar JR, Pejler G, Turk V, Turk B (2007) Glycosaminoglycans Facilitate Procathepsin B Activation through Disruption of Propeptide-Mature Enzyme Interactions. J Biol Chem 282: 33076-33085.
69. Novinec M, Grass RN, Stark WJ, Turk V, Baici A, et al. (2007) Interaction between human cathepsins K, L and S and elastins: mechanism of elastinolysis and inhibition by macromolecular inhibitors. J Biol Chem 282: 7893-7902.
70. Roughley PJ, Barrett AJ (1977) The degradation of cartilage proteoglycans by tissue proteinases. Proteoglycan structure and its susceptibility to proteolysis. Biochem J 167: 629-637.
71. Schenker P, Baici A (2010) Paradoxical interactions between modifiers and elastase-2. FEBS J 277: 2486-2495.