Collagenolytic activities of the major secreted cathepsin L peptidases involved in the virulence of the helminth pathogen, fasciola hepatica

PLoS Neglected Tropical Diseases

Volumn 5, Issue 4, 2011, Pages

  Robinson, Mark W ^a   Corvo, Ileana ^b   Jones, Peter M ^a   George, Anthony M ^a   Padula, Matthew P ^a   To, Joyce ^a   Cancela, Martin ^b,d   Rinaldi, Gabriel ^b,e   Tort, Jose F ^b   Roche, Leda ^b   Dalton, John P ^c  

^a UNIVERSITY OF TECHNOLOGY SYDNEY   (Australia)

^b DEPARTAMENTO DE BIOQUÍMICA   (Uruguay)

^c MCGILL UNIVERSITY   (Canada)

^d FEDERAL UNIVERSITY OF RIO GRANDE DO SUL   (Brazil)

^e GEORGE WASHINGTON UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CATHEPSIN L; CATHEPSIN L1; CATHEPSIN L3; CATHEPSIN V; COLLAGEN TYPE 1; COLLAGEN TYPE 2; COLLAGENASE; UNCLASSIFIED DRUG; COLLAGEN; HELMINTH PROTEIN; VIRULENCE FACTOR;

AMINO ACID SEQUENCE; ARTICLE; CONTROLLED STUDY; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME PURIFICATION; ENZYME RELEASE; FASCIOLA HEPATICA; HYDROLYSIS; MOLECULAR DYNAMICS; NONHUMAN; PARASITE VIRULENCE; PROTEIN CLEAVAGE; PROTEIN DOMAIN; PROTEIN EXPRESSION; SIMULATION; ANIMAL; CHEMICAL STRUCTURE; ENZYME SPECIFICITY; ENZYMOLOGY; KINETICS; METABOLISM; PATHOGENICITY; VIRULENCE;

ANIMALS; CATALYTIC DOMAIN; CATHEPSIN L; COLLAGEN; FASCIOLA HEPATICA; HELMINTH PROTEINS; KINETICS; MODELS, MOLECULAR; SUBSTRATE SPECIFICITY; VIRULENCE; VIRULENCE FACTORS;

EID: 79955874678     PISSN: 19352727     EISSN: 19352735     Source Type: Journal    
DOI: 10.1371/journal.pntd.0001012     Document Type: Article

References (59)

1. Robinson MW, Dalton JP, Donnelly S, (2008) Helminth pathogen cathepsin proteases: it's a family affair. Trends Biochem Sci 33: 601-608.
2. McGonigle L, Mousley A, Marks NJ, Brennan GP, Dalton JP, et al. (2008) The silencing of cysteine proteases in Fasciola hepatica newly excysted juveniles using RNA interference reduces gut penetration. Int J Parasitol 38: 149-155.
3. Lowther J, Robinson MW, Donnelly SM, Xu W, Stack CM, et al. (2009) The importance of pH in regulating the function of Fasciola hepatica cathepsin L1 cysteine protease. PLoS Negl Trop Dis 3: e369.
4. Sripa J, Laha T, To J, Brindley PJ, Sripa B, et al. (2010) Secreted cysteine proteases of the carcinogenic liver fluke, Opisthorchis viverrini: regulation of cathepsin F activation by autocatalysis and trans-processing by cathepsin B. Cell Microbiol 12: 781-795.
5. Smith AM, Dowd AJ, Heffernan M, Robertson CD, Dalton JP, (1993) Fasciola hepatica: a secreted cathepsin L-like proteinase cleaves host immunoglobulin. Int J Parasitol 23: 977-983.
6. Berasain P, Carmona C, Frangione B, Dalton JP, Goni F, (2000) Fasciola hepatica: parasite-secreted proteinases degrade all human IgG subclasses: determination of the specific cleavage sites and identification of the immunoglobulin fragments produced. Exp Parasitol 94: 99-110.
7. Donnelly S, O'Neill SM, Stack CM, Robinson MW, Turnbull L, et al. (2010) Helminth cysteine proteases inhibit TRIF-dependent activation of macrophages via degradation of TLR3. J Biol Chem 285: 3383-3392.
8. Dalton JP, Neill SO, Stack C, Collins P, Walshe A, et al. (2003) Fasciola hepatica cathepsin L-like proteases: biology, function, and potential in the development of first generation liver fluke vaccines. Int J Parasitol 33: 1173-1181.
9. Abdulla MH, Lim KC, Sajid M, McKerrow JH, Caffrey CR, (2007) Schistosomiasis mansoni: novel chemotherapy using a cysteine protease inhibitor. PLoS Med 4: e14.
10. Robinson MW, Dalton JP, (2009) Zoonotic helminth infections with particular emphasis on fasciolosis and other trematodiases. Phil Trans Royal Soc B 364: 2763-2776.
11. Keiser J, Utzinger J, (2005) Emerging foodborne trematodiasis. Emerg Infect Dis 11: 1507-1514.
12. Andrews SJ, (1999) The life-cycle of Fasciola hepatica. In: Dalton JP, editors. Fasciolosis CABI: Oxford, United Kingdom pp. 1-29.
13. Cancela M, Acosta D, Rinaldi G, Silva E, Durán R, et al. (2008) A distinctive repertoire of cathepsins is expressed by juvenile invasive Fasciola hepatica. Biochimie 90: 1461-1475.
14. Robinson MW, Tort JF, Wong E, Donnelly SM, Lowther J, et al. (2008) Proteomic and phylogenetic analysis of the cathepsin L protease family of the helminth pathogen, Fasciola hepatica: expansion of a repertoire of virulence-associated factors. Mol Cell Proteomics 7: 1111-1123.
15. Irving JA, Spithill TW, Pike RN, Whisstock JC, Smooker PM, (2003) The evolution of enzyme specificity in Fasciola spp. J Mol Evol 57: 1-15.
16. Robinson MW, Menon R, Donnelly SM, Dalton JP, Ranganathan S, (2009) An integrated transcriptomic and proteomic analysis of the secretome of the helminth pathogen, Fasciola hepatica: proteins associated with invasion and infection of the mammalian host. Mol Cell Proteomics 8: 1891-1907.
17. Cancela M, Ruetalo N, Dell'Oca N, da Silva E, Smircich P, et al. (2010) Survey of transcripts expressed by the invasive juvenile stage of the liver fluke Fasciola hepatica. BMC Genomics 11: 227.
18. Young ND, Hall RS, Jex AR, Cantacessi C, Gasser RB, (2010) Elucidating the transcriptome of Fasciola hepatica - a key to fundamental and biotechnological discoveries for a neglected parasite. Biotechnol Adv 28: 222-231.
19. Collins PR, Stack CM, O'Neill SM, Doyle S, Ryan T, et al. (2004) Cathepsin L1, the major protease involved in liver fluke (Fasciola hepatica) virulence: propetide cleavage sites and autoactivation of the zymogen secreted from gastrodermal cells. J Biol Chem 279: 17038-17046.
20. Na BK, Kim SH, Lee EG, Kim TS, Bae YA, et al. (2006) Critical roles for excretory-secretory cysteine proteases during tissue invasion of Paragonimus westermani newly excysted metacercariae. Cell Microbiol 8: 1034-1046.
21. Na BK, Kang JM, Sohn WM, (2008) CsCF-6, a novel cathepsin F-like cysteine protease for nutrient uptake of Clonorchis sinensis. Int J Parasitol 38: 493-502.
22. Stack CM, Caffrey CR, Donnelly SM, Seshaadri A, Lowther J, et al. (2008) Structural and functional relationships in the virulence-associated cathepsin L proteases of the parasitic liver fluke, Fasciola hepatica. J Biol Chem 283: 9896-9908.
23. Corvo I, Cancela M, Cappetta M, Pi-Denis N, Tort JF, et al. (2009) The major cathepsin L secreted by the invasive juvenile Fasciola hepatica prefers proline in the S2 subsite and can cleave collagen. Mol Biochem Parasitol 167: 41-47.
24. Turk D, Guncar G, Podobnik M, Turk B, (1998) Revised definition of substrate binding sites of papain-like cysteine proteases. Biol Chem 379: 137-147.
25. Turk D, Guncar G, (2003) Lysosomal cysteine proteases (cathepsins): promising drug targets. Acta Crystallogr D Biol Crystallogr 59: 203-213.
26. Atley LM, Mort JS, Lalumiere M, Eyre DR, (2000) Proteolysis of human bone collagen by cathepsin K: characterization of the cleavage sites generating the cross-linked N-telopeptide neoepitope. Bone 26: 241-247.
27. Gordon MK, Hahn RA, (2010) Collagens. Cell Tissue Res 339: 247-257.
28. Smooker PM, Whisstock JC, Irving JA, Siyaguna S, Spithill TW, et al. (2000) A single amino acid substitution affects substrate specificity in cysteine proteinases from Fasciola hepatica. Protein Sci 9: 2567-2572.
29. Kim M, Hamilton SE, Guddat LW, Overall CM, (2007) Plant collagenase: Unique collagenolytic activity of cysteine proteases from ginger. Biochim Biophys Acta 1770: 1627-1635.
30. Rawlings ND, Morton FR, Barrett AJ, (2006) MEROPS: The peptidase database. Nucleic Acids Res 34: D270-272.
31. Marquis RW, Ru Y, LoCastro SM, Zeng J, Yamashita DS, et al. (2001) Azepanone-Based Inhibitors of Human and Rat Cathepsin K. J Med Chem 44: 1380-1395.
32. Stern I, Schaschke N, Moroder L, Turk D, (2004) Crystal structure of NS-134 in complex with bovine cathepsin B: a two-headed epoxysuccinyl inhibitor extends along the entire active-site cleft. Biochem J 381: 511-517.
33. Guex N, Peitsch MC, (1997) SWISS-MODEL and the Swiss-PdbViewer: An environment for comparative protein modeling. Electrophoresis 18: 2714-2723.
34. Phillips JC, Braun R, Wang W, Gumbart J, Tajkhorshid E, et al. (2005) Scalable molecular dynamics with NAMD. J Comput Chem 26: 1781-1802.
35. Mezei M, (1997) Optimal Position of the Solute for Simulations. J Comp Chem 18: 812-815.
36. MacKerell AD, Feig M, Brooks CL, (2004) Extending the treatment of backbone energetics in protein force fields: limitations of gas-phase quantum mechanics in reproducing protein conformational distributions in molecular dynamics simulations. J Comput Chem 25: 1400-1415.
37. Veld PJ, Stevens MJ, (2008) Simulation of the Mechanical Strength of a Single Collagen Molecule. Biophys J 95: 33-39.
38. Jorgensen WL, Chandrasekhar J, Madura JD, Impey RW, Klein ML, (1983) Comparison of simple potential functions for simulating liquid water. J Chem Phys 79: 926-935.
39. Martyna GJ, Tobias DJ, Klein ML, (1994) Constant pressure molecular dynamics algorithms. J Chem Phys 101: 4177-4189.
40. Feller SE, Zhang YH, Pastor RW, Brooks BR, (1995) Constant pressure molecular dynamics simulation- the Langevin piston method. J Chem Phys 103: 4613-4621.
41. Darden T, York D, Pedersen L, (1993) Particle mesh Ewald. An N log(N) method for Ewald sums in large systems. J Chem Phys 98: 10089-10092.
42. Ryckaert JP, Ciccotti G, Berendsen HJC, (1977) Numerical integration of the Cartesian equations of motion of a system with constraints: molecular dynamics of n-alkanes. J Comp Phys 23: 327-341.
43. Miyamoto S, Kollman PA, (1992) SETTLE: An analytical version of the SHAKE and RATTLE algorithm for rigid water molecules. J Comput Chem 13: 952-962.
44. Wang W, Donini O, Reyes CM, Kollman PA, (2001) Biomolecular simulations: Recent developments in force fields, simulations of enzyme catalysis, protein-ligand, protein-protein, and protein-nucleic acid noncovalent interactions. Annu Rev Biophys Biomol Struct 30: 211-243.
45. Stoica I, Sadiq SK, Coveney PV, (2008) Rapid and accurate prediction of binding free energies of saquinavir-bound HIV-1 proteases. J Am Chem Soc 130: 2639-2648.
46. Case DA, Cheatham T, Darden T, Gohlke H, Luo R, et al. (2005) The Amber biomolecular simulation programs. J Comput Chem 26: 1668-1688.
47. Duan Y, Wu C, Chowdhury S, Lee MC, Xiong G, et al. (2003) A point-charge force field for molecular mechanics simulations of proteins based on condensed phase quantum mechanical calculations. J Comput Chem 24: 1999-2012.
48. Sanner MF, Olson AJ, Spehner JC, (1996) Reduced surface: an efficient way to compute molecular surfaces Biopolymers 38: 305-320.
49. Humphrey W, Dalke A, Schulten K, (1996) VMD: visual molecular dynamics. J Mol Graph 14: 33-38.
50. DeLano WL, (2002) The PyMOL Molecular Graphics System (Delano Scientific, San Carlos, California). Available: http://www.pymol.org. Accessed 2010.
51. Green GD, Shaw E, (1981) Peptidyl diazomethyl ketones are specific inactivators of thiol proteinases. J Biol Chem 256: 1923-1928.
52. Kirschke H, Shaw E, (1981) Rapid interaction of cathepsin L by Z-Phe-PheCHN12 and Z-Phe-AlaCHN2. Biochem Biophys Res Commun 101: 454-458.
53. Wang D, Pechar M, Li W, Kopecková P, Brömme D, et al. (2002) Inhibition of cathepsin K with lysosomotropic macromolecular inhibitors. Biochemistry 41: 8849-8859.
54. Schechter I, Berger A, (1968) On the size of the active site in proteases. I. Papain. Biochem Biophys Res Commun 27: 157-162.
55. Schwartz SD, Schramm VL, (2009) Enzymatic transition states and dynamic motion in barrier crossing. Nat Chem Biol 5: 551-558.
56. Kafienah W, Bromme D, Buttle DJ, Croucher LJ, Hollander AP, (1998) Human cathepsin K cleaves native type I and II collagens at the N-terminal end of the triple helix. Biochem J 331: 727-732.
57. Krane SM, (2008) The importance of proline residues in the structure, stability and susceptibility to proteolytic degradation of collagens. Amino Acids 35: 703-710.
58. Choi KH, Laursen RA, Allen KN, (1999) The 2.1 A structure of a cysteine protease with proline specificity from ginger rhizome, Zingiber officinale. Biochemistry 38: 11624-11633.
59. Wilson S, Hashamiyan S, Clarke L, Saftig P, Mort J, et al. (2009) Glycosaminoglycan-mediated loss of cathepsin K collagenolytic activity in MPS I contributes to osteoclast and growth plate abnormalities. Am J Pathol 175: 2053-2062.