1mmb › Citations

Structure determination and analysis of human neutrophil collagenase complexed with a hydroxamate inhibitor.

Grams F, Crimmin M, Hinnes L, Huxley P, Pieper M, Tschesche H, Bode W
Biochemistry 34 14012-20 (1995)
Cited: 71 times
EuropePMC logo PMID: 7577999

Abstract

Matrix metalloproteinases are a family of zinc endopeptidases involved in tissue remodeling. They have been implicated in various disease processes including metastasis, joint destruction, and neurodegeneration. Human neutrophil collagenase (HNC, MMP-8) represents one of the three "interstitial" collagenases that cleave triple-helical collagens types I, II, and III. Its 163-residue catalytic domain (Met80 to Gly242) has been expressed in Escherichia coli and crystallized as a noncovalent complex with the hydroxamate inhibitor batimastat. The crystal structure, refined to 2.1 A, demonstrates that batimastat binds to the S1-S2' sites and coordinates to the catalytic zinc in a bidentate manner via the hydroxyl and carbonyl oxygens of the hydroxamate group. The batimastat-collagenase complex is described in detail, and the activities of batimastat analogues are discussed in the light of the protein-inhibitor interactions revealed by the crystallography studies.

Articles - 1mmb mentioned but not cited (7)

  1. Database of traditional Chinese medicine and its application to studies of mechanism and to prescription validation. Chen X, Zhou H, Liu YB, Wang JF, Li H, Ung CY, Han LY, Cao ZW, Chen YZ. Br J Pharmacol 149 1092-1103 (2006)
  2. Development of quantitative structure-binding affinity relationship models based on novel geometrical chemical descriptors of the protein-ligand interfaces. Zhang S, Golbraikh A, Tropsha A. J Med Chem 49 2713-2724 (2006)
  3. Bioinformatic screening of autoimmune disease genes and protein structure prediction with FAMS for drug discovery. Ishida S, Umeyama H, Iwadate M, Taguchi YH. Protein Pept Lett 21 828-839 (2014)
  4. A comparison of the binding sites of matrix metalloproteinases and tumor necrosis factor-alpha converting enzyme: implications for selectivity. Lukacova V, Zhang Y, Kroll DM, Raha S, Comez D, Balaz S. J Med Chem 48 2361-2370 (2005)
  5. Dynamic clustering threshold reduces conformer ensemble size while maintaining a biologically relevant ensemble. Yongye AB, Bender A, Martínez-Mayorga K. J Comput Aided Mol Des 24 675-686 (2010)
  6. Preference of small molecules for local minimum conformations when binding to proteins. Wang Q, Pang YP. PLoS One 2 e820 (2007)
  7. Analysis of X-ray structures of matrix metalloproteinases via chaotic map clustering. Giangreco I, Nicolotti O, Carotti A, De Carlo F, Gargano G, Bellotti R. BMC Bioinformatics 11 500 (2010)


Reviews citing this publication (13)

  1. Critical appraisal of the use of matrix metalloproteinase inhibitors in cancer treatment. Zucker S, Cao J, Chen WT. Oncogene 19 6642-6650 (2000)
  2. Structural aspects of the metzincin clan of metalloendopeptidases. Gomis-Rüth FX. Mol Biotechnol 24 157-202 (2003)
  3. Insights into MMP-TIMP interactions. Bode W, Fernandez-Catalan C, Grams F, Gomis-Rüth FX, Nagase H, Tschesche H, Maskos K. Ann N Y Acad Sci 878 73-91 (1999)
  4. Future challenges facing the development of specific active-site-directed synthetic inhibitors of MMPs. Cuniasse P, Devel L, Makaritis A, Beau F, Georgiadis D, Matziari M, Yiotakis A, Dive V. Biochimie 87 393-402 (2005)
  5. Matrix metalloproteinase inhibitors: present achievements and future prospects. Denis LJ, Verweij J. Invest New Drugs 15 175-185 (1997)
  6. Experimental and clinical studies on the use of matrix metalloproteinase inhibitors for the treatment of cancer. Talbot DC, Brown PD. Eur J Cancer 32A 2528-2533 (1996)
  7. Matrix metalloproteinase inhibitors. Brown PD. Breast Cancer Res Treat 52 125-136 (1998)
  8. Clinical studies with matrix metalloproteinase inhibitors. Brown PD. APMIS 107 174-180 (1999)
  9. Structural basis of matrix metalloproteinases and tissue inhibitors of metalloproteinases. Maskos K, Bode W. Mol Biotechnol 25 241-266 (2003)
  10. Matrix metalloproteases: variations on a theme. Borkakoti N. Prog Biophys Mol Biol 70 73-94 (1998)
  11. Therapeutic potential of matrix metalloproteinases in Duchenne muscular dystrophy. Ogura Y, Tajrishi MM, Sato S, Hindi SM, Kumar A. Front Cell Dev Biol 2 11 (2014)
  12. Endoproteinase-protein inhibitor interactions. Bode W, Fernandez-Catalan C, Nagase H, Maskos K. APMIS 107 3-10 (1999)
  13. Structure-based organic synthesis of drug prototypes: a personal odyssey. Hanessian S. ChemMedChem 1 1301-1330 (2006)

Articles citing this publication (51)

  1. Structures of a histone deacetylase homologue bound to the TSA and SAHA inhibitors. Finnin MS, Donigian JR, Cohen A, Richon VM, Rifkind RA, Marks PA, Breslow R, Pavletich NP. Nature 401 188-193 (1999)
  2. Ongoing trials with matrix metalloproteinase inhibitors. Brown PD. Expert Opin Investig Drugs 9 2167-2177 (2000)
  3. Crystal structures of MMP-9 complexes with five inhibitors: contribution of the flexible Arg424 side-chain to selectivity. Tochowicz A, Maskos K, Huber R, Oltenfreiter R, Dive V, Yiotakis A, Zanda M, Pourmotabbed T, Bode W, Goettig P. J Mol Biol 371 989-1006 (2007)
  4. Batimastat, a potent matrix mealloproteinase inhibitor, exhibits an unexpected mode of binding. Botos I, Scapozza L, Zhang D, Liotta LA, Meyer EF. Proc Natl Acad Sci U S A 93 2749-2754 (1996)
  5. A combination of docking, QM/MM methods, and MD simulation for binding affinity estimation of metalloprotein ligands. Khandelwal A, Lukacova V, Comez D, Kroll DM, Raha S, Balaz S. J Med Chem 48 5437-5447 (2005)
  6. Collagenolytic and gelatinolytic matrix metalloproteinases and their inhibitors in basal cell carcinoma of skin: comparison with normal skin. Varani J, Hattori Y, Chi Y, Schmidt T, Perone P, Zeigler ME, Fader DJ, Johnson TM. Br J Cancer 82 657-665 (2000)
  7. Matrix metalloproteinase inhibitor batimastat alleviates pathology and improves skeletal muscle function in dystrophin-deficient mdx mice. Kumar A, Bhatnagar S, Kumar A. Am J Pathol 177 248-260 (2010)
  8. Substrate specificity determinants of human macrophage elastase (MMP-12) based on the 1.1 A crystal structure. Lang R, Kocourek A, Braun M, Tschesche H, Huber R, Bode W, Maskos K. J Mol Biol 312 731-742 (2001)
  9. Pyrimidine-2,4,6-Triones: a new effective and selective class of matrix metalloproteinase inhibitors. Grams F, Brandstetter H, D'Alò S, Geppert D, Krell HW, Leinert H, Livi V, Menta E, Oliva A, Zimmermann G, Gram F, Brandstetter H, D'Alò S, Geppert D, Krell HW, Leinert H, Livi VMenta E, Oliva A, Zimmermann G. Biol Chem 382 1277-1285 (2001)
  10. Shedding of discoidin domain receptor 1 by membrane-type matrix metalloproteinases. Fu HL, Sohail A, Valiathan RR, Wasinski BD, Kumarasiri M, Mahasenan KV, Bernardo MM, Tokmina-Roszyk D, Fields GB, Mobashery S, Fridman R. J Biol Chem 288 12114-12129 (2013)
  11. Crystal structures of novel non-peptidic, non-zinc chelating inhibitors bound to MMP-12. Morales R, Perrier S, Florent JM, Beltra J, Dufour S, De Mendez I, Manceau P, Tertre A, Moreau F, Compere D, Dublanchet AC, O'Gara M. J Mol Biol 341 1063-1076 (2004)
  12. A practical approach to docking of zinc metalloproteinase inhibitors. Hu X, Balaz S, Shelver WH. J Mol Graph Model 22 293-307 (2004)
  13. 1.8-A crystal structure of the catalytic domain of human neutrophil collagenase (matrix metalloproteinase-8) complexed with a peptidomimetic hydroxamate primed-side inhibitor with a distinct selectivity profile. Betz M, Huxley P, Davies SJ, Mushtaq Y, Pieper M, Tschesche H, Bode W, Gomis-Rüth FX. Eur J Biochem 247 356-363 (1997)
  14. Amber force field implementation, molecular modelling study, synthesis and MMP-1/MMP-2 inhibition profile of (R)- and (S)-N-hydroxy-2-(N-isopropoxybiphenyl-4-ylsulfonamido)-3-methylbutanamides. Tuccinardi T, Martinelli A, Nuti E, Carelli P, Balzano F, Uccello-Barretta G, Murphy G, Rossello A. Bioorg Med Chem 14 4260-4276 (2006)
  15. Crystal structure of the stromelysin catalytic domain at 2.0 A resolution: inhibitor-induced conformational changes. Chen L, Rydel TJ, Gu F, Dunaway CM, Pikul S, Dunham KM, Barnett BL. J Mol Biol 293 545-557 (1999)
  16. Structural characterizations of nonpeptidic thiadiazole inhibitors of matrix metalloproteinases reveal the basis for stromelysin selectivity. Finzel BC, Baldwin ET, Bryant GL, Hess GF, Wilks JW, Trepod CM, Mott JE, Marshall VP, Petzold GL, Poorman RA, O'Sullivan TJ, Schostarez HJ, Mitchell MA. Protein Sci 7 2118-2126 (1998)
  17. Crystal structure of the catalytic domain of MMP-16/MT3-MMP: characterization of MT-MMP specific features. Lang R, Braun M, Sounni NE, Noel A, Frankenne F, Foidart JM, Bode W, Maskos K. J Mol Biol 336 213-225 (2004)
  18. N-Hydroxyurea as zinc binding group in matrix metalloproteinase inhibition: mode of binding in a complex with MMP-8. Campestre C, Agamennone M, Tortorella P, Preziuso S, Biasone A, Gavuzzo E, Pochetti G, Mazza F, Hiller O, Tschesche H, Consalvi V, Gallina C. Bioorg Med Chem Lett 16 20-24 (2006)
  19. Phosph(on)ate as a zinc-binding group in metalloenzyme inhibitors: X-ray crystal structure of the antiviral drug foscarnet complexed to human carbonic anhydrase I. Temperini C, Innocenti A, Guerri A, Scozzafava A, Rusconi S, Supuran CT. Bioorg Med Chem Lett 17 2210-2215 (2007)
  20. Carbonic anhydrase inhibitors: inhibition of cytosolic/tumor-associated isoforms I, II, and IX with iminodiacetic carboxylates/hydroxamates also incorporating benzenesulfonamide moieties. Santos MA, Marques S, Vullo D, Innocenti A, Scozzafava A, Supuran CT. Bioorg Med Chem Lett 17 1538-1543 (2007)
  21. Hydroxyurea is a carbonic anhydrase inhibitor. Scozzafava A, Supuran CT. Bioorg Med Chem 11 2241-2246 (2003)
  22. Design and characterization of a metalloproteinase inhibitor-tethered resin for the detection of active MMPs in biological samples. Hesek D, Toth M, Meroueh SO, Brown S, Zhao H, Sakr W, Fridman R, Mobashery S. Chem Biol 13 379-386 (2006)
  23. Picking the S1, S1' and S2' pockets of matrix metalloproteinases. A niche for potent acyclic sulfonamide inhibitors. Hanessian S, Bouzbouz S, Boudon A, Tucker GC, Peyroulan D. Bioorg Med Chem Lett 9 1691-1696 (1999)
  24. Structure of malonic acid-based inhibitors bound to human neutrophil collagenase. A new binding mode explains apparently anomalous data. Brandstetter H, Engh RA, Von Roedern EG, Moroder L, Huber R, Bode W, Grams F. Protein Sci 7 1303-1309 (1998)
  25. 2 angstrom X-ray structure of adamalysin II complexed with a peptide phosphonate inhibitor adopting a retro-binding mode. Cirilli M, Gallina C, Gavuzzo E, Giordano C, Gomis-Rüth FX, Gorini B, Kress LF, Mazza F, Paradisi MP, Pochetti G, Politi V. FEBS Lett 418 319-322 (1997)
  26. N-hydroxyurea--a versatile zinc binding function in the design of metalloenzyme inhibitors. Temperini C, Innocenti A, Scozzafava A, Supuran CT. Bioorg Med Chem Lett 16 4316-4320 (2006)
  27. Structural differences of matrix metalloproteinases. Homology modeling and energy minimization of enzyme-substrate complexes. Terp GE, Christensen IT, Jørgensen FS. J Biomol Struct Dyn 17 933-946 (2000)
  28. Protease inhibitors - part 5. Alkyl/arylsulfonyl- and arylsulfonylureido-/arylureido- glycine hydroxamate inhibitors of Clostridium histolyticum collagenase. Scozzafava A, Supuran CT. Eur J Med Chem 35 299-307 (2000)
  29. Tetrahydroisoquinoline-3-carboxylate based matrix-metalloproteinase inhibitors: design, synthesis and structure-activity relationship. Matter H, Schudok M, Schwab W, Thorwart W, Barbier D, Billen G, Haase B, Neises B, Weithmann K, Wollmann T. Bioorg Med Chem 10 3529-3544 (2002)
  30. A comparative docking study and the design of potentially selective MMP inhibitors. Hanessian S, Moitessier N, Therrien E. J Comput Aided Mol Des 15 873-881 (2001)
  31. The interaction of zinc(II) and hydroxamic acids and a metal-triggered Lossen rearrangement. Duchácková L, Roithová J. Chemistry 15 13399-13405 (2009)
  32. Characterization of a metalloproteinase: a late stage specific gelatinase activity in the sea urchin embryo. Robinson JJ. J Cell Biochem 66 337-345 (1997)
  33. Solution structures of stromelysin complexed to thiadiazole inhibitors. Stockman BJ, Waldon DJ, Gates JA, Scahill TA, Kloosterman DA, Mizsak SA, Jacobsen EJ, Belonga KL, Mitchell MA, Mao B, Petke JD, Goodman L, Powers EA, Ledbetter SR, Kaytes PS, Vogeli G, Marshall VP, Petzold GL, Poorman RA. Protein Sci 7 2281-2286 (1998)
  34. The design, synthesis, and structure-activity relationships of a series of macrocyclic MMP inhibitors. Steinman DH, Curtin ML, Garland RB, Davidsen SK, Heyman HR, Holms JH, Albert DH, Magoc TJ, Nagy IB, Marcotte PA, Li J, Morgan DW, Hutchins C, Summers JB. Bioorg Med Chem Lett 8 2087-2092 (1998)
  35. Effect of species differences on stromelysin-1 (MMP-3) inhibitor potency. An explanation of inhibitor selectivity using homology modeling and chimeric proteins. Johnson LL, Bornemeier DA, Janowicz JA, Chen J, Pavlovsky AG, Ortwine DF. J Biol Chem 274 24881-24887 (1999)
  36. Hydroxamate derivatives of substrate-analogous peptides containing aminomalonic acid are potent inhibitors of matrix metalloproteinases. Krumme D, Wenzel H, Tschesche H. FEBS Lett 436 209-212 (1998)
  37. Inhibition of arginine gingipains (RgpB and HRgpA) with benzamidine inhibitors: zinc increases inhibitory potency. Krauser JA, Potempa J, Travis J, Powers JC. Biol Chem 383 1193-1198 (2002)
  38. Design and synthesis of dual inhibitors for matrix metalloproteinase and cathepsin. Yamamoto M, Ikeda S, Kondo H, Inoue S. Bioorg Med Chem Lett 12 375-378 (2002)
  39. Protease inhibitors. Part 12. Synthesis of potent matrix metalloproteinase and bacterial collagenase inhibitors incorporating sulfonylated N-4-nitrobenzyl-beta-alanine hydroxamate moieties. Scozzafava A, Ilies MA, Manole G, Supuran CT. Eur J Pharm Sci 11 69-79 (2000)
  40. Protease inhibitors. Part 8: synthesis of potent Clostridium histolyticum collagenase inhibitors incorporating sulfonylated L-alanine hydroxamate moieties. Scozzafava A, Supuran CT. Bioorg Med Chem 8 637-645 (2000)
  41. Protease inhibitors: Synthesis of L-alanine hydroxamate sulfonylated derivatives as inhibitors of clostridium histolyticum collagenase. Supuran CT, Briganti F, Mincione G, Scozzafava A. J Enzyme Inhib 15 111-128 (2000)
  42. Three-dimensional structure of fibrolase, the fibrinolytic enzyme from southern copperhead venom, modeled from the X-ray structure of adamalysin II and atrolysin C. Bolger MB, Swenson S, Markland FS. AAPS PharmSci 3 E16 (2001)
  43. Computational study of the catalytic domain of human neutrophil collagenase. specific role of the S3 and S'3 subsites in the interaction with a phosphonate inhibitor. Aschi M, Roccatano D, Di Nola A, Gallina C, Gavuzzo E, Pochetti G, Pieper M, Tschesche H, Mazza F. J Comput Aided Mol Des 16 213-225 (2002)
  44. Novel hydroxamic acid-related phosphinates: inhibition of neutral aminopeptidase N (APN). Drag M, Grzywa R, Oleksyszyn J. Bioorg Med Chem Lett 17 1516-1519 (2007)
  45. QM/MM linear response method distinguishes ligand affinities for closely related metalloproteins. Khandelwal A, Balaz S. Proteins 69 326-339 (2007)
  46. Non-peptidic cysteine derivatives as inhibitors of matrix metalloproteinases. Müller JC, von Roedern EG, Grams F, Nagase H, Moroder L. Biol Chem 378 1475-1480 (1997)
  47. Selective inhibition of low affinity IgE receptor (CD23) processing. Bailey S, Bolognese B, Buckle DR, Faller A, Jackson S, Louis-Flamberg P, McCord M, Mayer RJ, Marshall LA, Smith DG. Bioorg Med Chem Lett 8 29-34 (1998)
  48. Structural and spectroscopic studies of tripodal [MgL]2+ chelates containing only nitrogen donor atoms: alkaline earth metal complexes as potential drug delivery agents. He H, Rodgers KR, Arif AM. J Inorg Biochem 98 667-676 (2004)
  49. The constituent tryptophans and bisANS as fluorescent probes of the active site and of a secondary binding site of stromelysin-1 (MMP-3). Epps DE, Poorman RA, Petzold GL, Stuchly CW, Laborde AL, Van Drie JH. J Protein Chem 17 699-712 (1998)
  50. Fluorescent Analogue of Batimastat Enables Imaging of α-Secretase in Living Cells. Leriche G, Chen AC, Kim S, Selkoe DJ, Yang J. ACS Chem Neurosci 7 40-45 (2016)
  51. A fluorescence resonance energy transfer method for measuring the binding of inhibitors to stromelysin. Epps DE, Mitchell MA, Petzold GL, VanDrie JH, Poorman RA. Anal Biochem 275 141-147 (1999)


Related citations provided by authors (3)

  1. X-Ray Structures of Human Neutrophil Collagenase Complexed with Peptide Hydroxamate and Peptide Thiol Inhibitors. Implications for Substrate Binding and Rational Drug Design. Grams F, Reinemer P, Powers JC, Kleine T, Pieper M, Tschesche H, Huber R, Bode W Eur. J. Biochem. 228 830- (1995)
  2. Structural Implications for the Role of the N Terminus in the 'Superactivation' of Collagenases. A Crystallographic Study. Reinemer P, Grams F, Huber R, Kleine T, Schnierer S, Piper M, Tschesche H, Bode W FEBS Lett. 338 227- (1994)
  3. The X-Ray Crystal Structure of the Catalytic Domain of Human Neutrophil Collagenase Inhibited by a Substrate Analogue Reveals the Essentials for Catalysis and Specificity. Bode W, Reinemer P, Huber R, Kleine T, Schnierer S, Tschesche H EMBO J. 13 1263- (1994)

Quick links