Kinetic analysis and molecular modeling of the inhibition mechanism of roneparstat (SST0001) on human heparanase

Glycobiology

Volumn 26, Issue 6, 2016, Pages 640-654

  Pala, Daniele ^a   Rivara, Silvia ^a   Mor, Marco ^a   Milazzo, Ferdinando Maria ^b   Roscilli, Giuseppe ^c   Pavoni, Emiliano ^c   Giannini, Giuseppe ^b  

^a UNIVERSITY OF PARMA   (Italy)

^b Sigma Tau SpA   (Italy)

^c Takis srl   (Italy)

Author keywords

heparanase; homology modeling; kinetic inhibition analysis; roneparstat; SST0001

Indexed keywords

FONDAPARINUX; HEPARANASE; RONEPARSTAT; BETA GLUCURONIDASE; ENZYME INHIBITOR; HEPARIN; POLYSACCHARIDE; PROTEIN BINDING; RECOMBINANT PROTEIN;

ACIDOBACTERIUM CAPSULATUM; ARTICLE; BURKHOLDERIA PSEUDOMALLEI; COMPARATIVE STUDY; COMPETITIVE INHIBITION; CONFORMATION; CONSERVED SEQUENCE; CONTROLLED STUDY; CRYSTAL STRUCTURE; DRUG BINDING; DRUG MECHANISM; ENZYME INHIBITION; ENZYME SUBSTRATE COMPLEX; HUMAN; HYDROGEN BOND; IC50; KINETICS; LIGAND BINDING; MOLECULAR DOCKING; MOLECULAR MODEL; MOLECULAR WEIGHT; PRIORITY JOURNAL; SUBSTRATE CONCENTRATION; ACIDOBACTERIA; ALPHA HELIX; ANALOGS AND DERIVATIVES; ANTAGONISTS AND INHIBITORS; BETA SHEET; BINDING SITE; CARBOHYDRATE ANALYSIS; CHEMISTRY; ENZYME SPECIFICITY; ENZYMOLOGY; METABOLISM; MOLECULAR DYNAMICS; PROTEIN DOMAIN; PROTEIN MOTIF; STRUCTURAL HOMOLOGY; THERMODYNAMICS;

ACIDOBACTERIA; AMINO ACID MOTIFS; BINDING SITES; CARBOHYDRATE SEQUENCE; ENZYME INHIBITORS; GLUCURONIDASE; HEPARIN; HUMANS; KINETICS; MOLECULAR DOCKING SIMULATION; MOLECULAR DYNAMICS SIMULATION; POLYSACCHARIDES; PROTEIN BINDING; PROTEIN CONFORMATION, ALPHA-HELICAL; PROTEIN CONFORMATION, BETA-STRAND; PROTEIN INTERACTION DOMAINS AND MOTIFS; RECOMBINANT PROTEINS; STRUCTURAL HOMOLOGY, PROTEIN; SUBSTRATE SPECIFICITY; THERMODYNAMICS;

EID: 84973352319     PISSN: 09596658     EISSN: 14602423     Source Type: Journal    
DOI: 10.1093/glycob/cww003     Document Type: Article

References (74)

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2. AckerMG, Auld DS. 2014. Considerations for the design and reporting of enzyme assays in high-throughput screening applications. Perspect Sci. 1:56-73.
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29. McKenzie EA. 2007. Heparanase: A target for drug discovery in cancer and inflammation. Br J Pharmacol. 151:1-14.
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32. Naggi A, Casu B, PerezM, Torri G, Cassinelli G, Penco S, Pisano C, Giannini G, Ishai-Michaeli R, Vlodavsky I. 2005. Modulation of the heparanaseinhibiting activity of heparin through selective desulfation, graded N-acetylation, glycol splitting. J Biol Chem. 280:12103-12113.
33. Nakajima M, Irimura T, Di Ferrante N, Nicolson GL. 1984. Metastatic melanoma cell heparanase. Characterization of heparan sulfate degradation fragments produced by B16 melanoma endoglucuronidase. J Biol Chem. 259:2283-2290.
34. Nardella C, Lahm A, PallaoroM, Brunetti M, Vannini A, Steinkühler C. 2004. Mechanism of activation of human heparanase investigated by protein engineering. Biochemistry (Mosc). 43:1862-1873.
35. Okada Y, Yamada S, Toyoshima M, Dong J, Nakajima M, Sugahara K. 2002. Structural recognition by recombinant human heparanase that plays critical roles in tumor metastasis. Hierarchical sulfate groups with different effects and the essential target disulfated trisaccharide sequence. J Biol Chem. 277:42488-42495.
36. Pikas DS, Li JP, Vlodavsky I, Lindahl U. 1998. Substrate specificity of heparanases from human hepatoma and platelets. J Biol Chem. 273:18770-18777.
37. Pisano C, Vlodavsky I, Ilan N, Zunino F. 2014. The potential of heparanase as a therapeutic target in cancer. Biochem Pharmacol. 89:12-19.
38. Abboud-Jarrous G, Atzmon R, Peretz T, Palermo C, Gadea BB, Joyce JA, Vlodavsky I. 2008. Cathepsin L is responsible for processing and activation of proheparanase through multiple cleavages of a linker segment. J Biol Chem. 283:18167-18176.
39. AckerMG, Auld DS. 2014. Considerations for the design and reporting of enzyme assays in high-throughput screening applications. Perspect Sci. 1:56-73.
40. Banks JL, Beard HS, Cao Y, Cho AE, DammW, Farid R, Felts AK, Halgren TA, Mainz DT, Maple JR, et al. 2005. Integrated modeling program, applied chemical theory (IMPACT). J Comput Chem. 26:1752-1780.
41. Basche M, Gustafson DL, Holden SN, O'Bryant CL, Gore L, Witta S, Schultz MK, Morrow M, Levin A, Creese BR, et al. 2006. A phase I biological and pharmacologic study of the heparanase inhibitor PI-88 in patients with advanced solid tumors. Clin Cancer Res Off J Am Assoc Cancer Res. 12:5471-5480.
42. Bohlmann L, Tredwell GD, Yu X, Chang C-W, Haselhorst T, Winger M, Dyason JC, Thomson RJ, Tiralongo J, Beacham IR, et al. 2015. Functional and structural characterization of a heparanase. Nat Chem Biol. 11:955-957.
43. Cao R, Zeidan AA, Rådström P, van Niel EWJ. 2010. Inhibition kinetics of catabolic dehydrogenases by elevated moieties of ATP and ADP ? Implication for a new regulation mechanism in Lactococcus lactis. FEBS J. 277:1843-1852.
44. Casu B, Vlodavsky I, Sanderson RD. 2008. Non-anticoagulant heparins and inhibition of cancer. Pathophysiol Haemost Thromb. 36:195-203.
45. Choay J, Petitou M, Lormeau JC, Sinaÿ P, Casu B, Gatti G. 1983. Structureactivity relationship in heparin: A synthetic pentasaccharide with high affinity for antithrombin III and eliciting high anti-factor Xa activity. Biochem Biophys Res Commun. 116:492-499.
46. Copeland RA. 2005. Evaluation of Enzyme Inhibitors in Drug Discovery. A Guide for Medicinal Chemists and Pharmacologists. 1st ed. Hoboken (NJ): John Wiley & Sons, Inc.
47. Davies GJ,Wilson KS, Henrissat B. 1997. Nomenclature for sugar-binding subsites in glycosyl hydrolases. Biochem J. 321(Pt 2):557-559.
48. D. E. Shaw Research. 2013. Desmond Molecular Dynamics System, Version 3.6, Maestro-Desmond Interoperability Tools, Version 3.6. New York (NY).
49. Dredge K, Hammond E, Handley P, Gonda TJ, Smith MT, Vincent C, Brandt R, Ferro V, Bytheway I. 2011. PG545, a dual heparanase and angiogenesis inhibitor, induces potent anti-tumour and anti-metastatic efficacy in preclinical models. Br J Cancer. 104:635-642.
50. Essmann U, Perera L, Berkowitz ML, Darden T, Lee H, Pedersen LG. 1995. A smooth particle mesh Ewald method. J Chem Phys. 103:8577.
51. Fan H, Mark AE. 2004. Refinement of homology-based protein structures by molecular dynamics simulation techniques. Protein Sci Publ Protein Soc. 13:211-220.
52. Feller SE, Zhang Y, Pastor RW, Brooks BR. 1995. Constant pressure molecular dynamics simulation: The Langevin piston method. J Chem Phys. 103:4613.
53. Ferro V. 2013. Heparan sulfate inhibitors and their therapeutic implications in inflammatory illnesses. Expert Opin Ther Targets. 17:965-975.
54. Ferro V, Hammond E, Fairweather JK. 2004. The development of inhibitors of heparanase, a key enzyme involved in tumour metastasis, angiogenesis and inflammation. Mini Rev Med Chem. 4:693-702.
55. Gandhi NS, Freeman C, Parish CR, Mancera RL. 2012. Computational analyses of the catalytic and heparin-binding sites and their interactions with glycosaminoglycans in glycoside hydrolase family 79 endo-?-D-glucuronidase (heparanase). Glycobiology. 22:35-55.
56. Hammond E, Handley P, Dredge K, Bytheway I. 2013. Mechanisms of heparanase inhibition by the heparan sulfate mimetic PG545 and three structural analogues. FEBS Open Bio. 3:346-351.
57. Hammond E, Li CP, Ferro V. 2010. Development of a colorimetric assay for heparanase activity suitable for kinetic analysis and inhibitor screening. Anal Biochem. 396:112-116.
58. Huegel J, Enomoto-Iwamoto M, Sgariglia F, Koyama E, Pacifici M. 2015. Heparanase stimulates chondrogenesis and is up-regulated in human ectopic cartilage: A mechanism possibly involved in hereditary multiple exostoses. Am J Pathol. 185:1676-1685.
59. Hulett MD, Hornby JR, Ohms SJ, Zuegg J, Freeman C, Gready JE, Parish CR. 2000. Identification of active-site residues of the pro-metastatic endoglycosidase heparanase. Biochemistry (Mosc). 39:15659-15667.
60. Kirschner KN, Yongye AB, Tschampel SM, González-Outeirinõ J, Daniels CR, Foley BL, Woods RJ. 2008. GLYCAM06: A generalizable biomolecular force field. Carbohydrates. J Comput Chem. 29: 622-655.
61. Kolossvàry I, Guida WC. 1999. Low-mode conformational search elucidated: Application to C39H80 and flexible docking of 9-deazaguanine inhibitors into PNP. J Comput Chem. 20:1671-1684.
62. Krautler V, van Gunsteren WF, Hunenberger PH. 2001. A fast SHAKE algorithm to solve distance constraint equations for small molecules in molecular dynamics simulations. J Comput Chem. 22:501-508.
63. Levy-Adam F, Abboud-Jarrous G, Guerrini M, Beccati D, Vlodavsky I, Ilan N. 2005. Identification and characterization of heparin/heparan sulfate binding domains of the endoglycosidase heparanase. J Biol Chem. 280:20457-20466.
64. Lindorff-Larsen K, Piana S, Palmo K, Maragakis P, Klepeis JL, Dror RO, Shaw DE. 2010. Improved side-chain torsion potentials for the Amber ff99SB protein force field. Proteins. 78:1950-1958.
65. Mao Y, Huang Y, Buczek-Thomas JA, Ethen CM, Nugent MA, Wu ZL, Zaia J. 2014. A liquid chromatography-mass spectrometry-based approach to characterize the substrate specificity of mammalian heparanase. J Biol Chem. 289:34141-34151.
66. McKenzie EA. 2007. Heparanase: A target for drug discovery in cancer and inflammation. Br J Pharmacol. 151:1-14.
67. Michikawa M, Ichinose H, Momma M, Biely P, Jongkees S, Yoshida M, Kotake T, Tsumuraya Y, Withers SG, Fujimoto Z, et al. 2012. Structural and biochemical characterization of glycoside hydrolase family 79 ?-glucuronidase from Acidobacterium capsulatum. J Biol Chem. 287:14069-14077.
68. Mulloy B, Forster MJ, Jones C, Davies DB. 1993. N.m.r., molecularmodelling studies of the solution conformation of heparin. Biochem J. 293(Pt 3):849-858.
69. Naggi A, Casu B, PerezM, Torri G, Cassinelli G, Penco S, Pisano C, Giannini G, Ishai-Michaeli R, Vlodavsky I. 2005. Modulation of the heparanaseinhibiting activity of heparin through selective desulfation, graded N-acetylation, glycol splitting. J Biol Chem. 280:12103-12113.
70. Nakajima M, Irimura T, Di Ferrante N, Nicolson GL. 1984. Metastatic melanoma cell heparanase. Characterization of heparan sulfate degradation fragments produced by B16 melanoma endoglucuronidase. J Biol Chem. 259:2283-2290.
71. Nardella C, Lahm A, PallaoroM, Brunetti M, Vannini A, Steinkühler C. 2004. Mechanism of activation of human heparanase investigated by protein engineering. Biochemistry (Mosc). 43:1862-1873.
72. Okada Y, Yamada S, Toyoshima M, Dong J, Nakajima M, Sugahara K. 2002. Structural recognition by recombinant human heparanase that plays critical roles in tumor metastasis. Hierarchical sulfate groups with different effects and the essential target disulfated trisaccharide sequence. J Biol Chem. 277:42488-42495.
73. Pikas DS, Li JP, Vlodavsky I, Lindahl U. 1998. Substrate specificity of heparanases from human hepatoma and platelets. J Biol Chem. 273:18770-18777.
74. Pisano C, Vlodavsky I, Ilan N, Zunino F. 2014. The potential of heparanase as a therapeutic target in cancer. Biochem Pharmacol. 89:12-19.