Structural analysis of inhibition of E. coli methionine aminopeptidase: Implication of loop adaptability in selective inhibition of bacterial enzymes

BMC Structural Biology

Volumn 7, Issue , 2007, Pages

  Ma, Ze Qiang ^a   Xie, Sheng Xue ^a   Huang, Qing Qing ^b   Nan, Fa Jun ^b   Hurley, Thomas D ^c   Ye, Qi Zhuang ^a,c  

^a UNIVERSITY OF KANSAS   (United States)

^b SHANGHAI INSTITUTE OF MATERIA MEDICA   (China)

^c INDIANA UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL ENZYME; METHIONYL AMINOPEPTIDASE; AMINOPEPTIDASE; ANTIINFECTIVE AGENT; GLYCINE; HISTIDINE; ISOENZYME; TYROSINE;

AMINO TERMINAL SEQUENCE; ARTICLE; ENZYME INHIBITION; ESCHERICHIA COLI; NONHUMAN; X RAY; BINDING SITE; CHEMICAL STRUCTURE; CHEMISTRY; DRUG ANTAGONISM; DRUG DESIGN; ENZYMOLOGY; HUMAN; METABOLISM; PROTEIN SECONDARY STRUCTURE; SENSITIVITY AND SPECIFICITY; X RAY CRYSTALLOGRAPHY;

BACTERIA (MICROORGANISMS);

AMINOPEPTIDASES; ANTI-BACTERIAL AGENTS; BINDING SITES; CRYSTALLOGRAPHY, X-RAY; DRUG DESIGN; ESCHERICHIA COLI; GLYCINE; HISTIDINE; HUMANS; ISOENZYMES; MODELS, MOLECULAR; PROTEIN STRUCTURE, SECONDARY; SENSITIVITY AND SPECIFICITY; TYROSINE;

EID: 38949190658     PISSN: None     EISSN: 14726807     Source Type: Journal    
DOI: 10.1186/1472-6807-7-84     Document Type: Article

References (51)

1. N-terminal processing: the methionine aminopeptidase and N alpha-acetyl transferase families. RA Bradshaw WW Brickey KW Walker, Trends Biochem Sci 1998 23 7 263 267 10.1016/S0968-0004(98)01227-4 9697417
2. Methionine aminopeptidase gene of Escherichia coli is essential for cell growth. SY Chang EC McGary S Chang, J Bacteriol 1989 171 7 4071 4072 2544569
3. pepM is an essential gene in Salmonella typhimurium. CG Miller AM Kukral JL Miller NR Movva, J Bacteriol 1989 171 9 5215 5217 2670909
4. Methionine in and out of proteins: targets for drug design. MD Vaughan PB Sampson JF Honek, Curr Med Chem 2002 9 3 385 409 11860363
5. Eukaryotic methionyl aminopeptidases: two classes of cobalt-dependent enzymes. SM Arfin RL Kendall L Hall LH Weaver AE Stewart BW Matthews RA Bradshaw, Proc Natl Acad Sci U S A 1995 92 17 7714 7718 7644482 10.1073/pnas.92.17.7714
6. Amino-terminal protein processing in Saccharomyces cerevisiae is an essential function that requires two distinct methionine aminopeptidases. X Li YH Chang, Proc Natl Acad Sci U S A 1995 92 26 12357 12361 8618900 10.1073/pnas.92.26.12357
7. Molecular recognition of angiogenesis inhibitors fumagillin and ovalicin by methionine aminopeptidase 2. EC Griffith Z Su S Niwayama CA Ramsay YH Chang JO Liu, Proc Natl Acad Sci U S A 1998 95 26 15183 15188 9860943 10.1073/pnas.95.26.15183
8. Methionine aminopeptidase (type 2) is the common target for angiogenesis inhibitors AGM-1470 and ovalicin. EC Griffith Z Su BE Turk S Chen YH Chang Z Wu K Biemann JO Liu, Chem Biol 1997 4 6 461 471 10.1016/S1074-5521(97)90198-8 9224570
9. The anti-angiogenic agent fumagillin covalently binds and inhibits the methionine aminopeptidase, MetAP-2. N Sin L Meng MQ Wang JJ Wen WG Bornmann CM Crews, Proc Natl Acad Sci U S A 1997 94 12 6099 6103 9177176 10.1073/pnas.94.12.6099
10. Proteomics-based target identification: bengamides as a new class of methionine aminopeptidase inhibitors. H Towbin KW Bair JA DeCaprio MJ Eck S Kim FR Kinder A Morollo DR Mueller P Schindler HK Song, J Biol Chem 2003 278 52 52964 52971 10.1074/jbc.M309039200 14534293
11. Synthesis of (3R)-amino-(2S)-hydroxy amino acids for inhibition of methionine aminopeptidase-1. SJ Keding NA Dales S Lim D Beauliu DH Rich, Synth Commun 1998 28 4463 4470 10.1080/00397919808004481
12. Insights into the mechanism of Escherichia coli methionine aminopeptidase from the structural analysis of reaction products and phosphorus-based transition-state analogues. WT Lowther Y Zhang PB Sampson JF Honek BW Matthews, Biochemistry 1999 38 45 14810 14819 10.1021/bi991711g 10555963
13. Escherichia coli methionine aminopeptidase: implications of crystallographic analyses of the native, mutant, and inhibited enzymes for the mechanism of catalysis. WT Lowther AM Orville DT Madden S Lim DH Rich BW Matthews, Biochemistry 1999 38 24 7678 7688 10.1021/bi990684r 10387007
14. Structural basis of catalysis by monometalated methionine aminopeptidase. QZ Ye SX Xie ZQ Ma M Huang RP Hanzlik, Proc Natl Acad Sci U S A 2006 103 25 9470 9475 16769889 10.1073/pnas.0602433103
15. Structure of human methionine aminopeptidase-2 complexed with fumagillin. S Liu J Widom CW Kemp CM Crews J Clardy, Science 1998 282 5392 1324 1327 10.1126/science.282.5392.1324 9812898
16. The anti-angiogenic agent fumagillin covalently modifies a conserved active-site histidine in the Escherichia coli methionine aminopeptidase. WT Lowther DA McMillen AM Orville BW Matthews, Proc Natl Acad Sci U S A 1998 95 21 12153 12157 9770455 10.1073/pnas.95.21.12153
17. Metalloform-selective inhibitors of escherichia coli methionine aminopeptidase and X-ray structure of a Mn(II)-form enzyme complexed with an inhibitor. QZ Ye SX Xie M Huang WJ Huang JP Lu ZQ Ma, J Am Chem Soc 2004 126 43 13940 13941 10.1021/ja045864p 15506752
18. Metalloform-selective inhibition: Synthesis and structure-activity analysis of Mn(II)-form-selective inhibitors of Escherichia coli methionine aminopeptidase. QQ Huang M Huang FJ Nan QZ Ye, Bioorg Med Chem Lett 2005 15 24 5386 5391 10.1016/j.bmcl.2005.09.019 16219464
19. Metal ions as cofactors for the binding of inhibitors to methionine aminopeptidase: A critical view of the relevance of in vitro metalloenzyme assays. R Schiffmann A Heine G Klebe CD Klein, Angew Chem Int Ed Engl 2005 44 23 3620 3623 10.1002/anie.200500592 15880695
20. Discovery and structural modification of inhibitors of methionine aminopeptidases from Escherichia coli and Saccharomyces cerevisiae. QL Luo JY Li ZY Liu LL Chen J Li Z Qian Q Shen Y Li GH Lushington QZ Ye, J Med Chem 2003 46 13 2631 2640 10.1021/jm0300532 12801227
21. Crystal structures of Staphylococcusaureus methionine aminopeptidase complexed with keto heterocycle and aminoketone inhibitors reveal the formation of a tetrahedral intermediate. A Douangamath GE Dale A D'Arcy M Almstetter R Eckl A Frutos-Hoener B Henkel K Illgen S Nerdinger H Schulz, J Med Chem 2004 47 6 1325 1328 10.1021/jm034188j 14998322
22. The 1.15A crystal structure of the Staphylococcus aureus methionyl-aminopeptidase and complexes with triazole based inhibitors. C Oefner A Douangamath A D'Arcy S Hafeli D Mareque A Mac Sweeney J Padilla S Pierau H Schulz M Thormann, J Mol Biol 2003 332 1 13 21 10.1016/S0022-2836(03)00862-3 12946343
23. Physiologically relevant metal cofactor for methionine aminopeptidase-2 is manganese. J Wang GS Sheppard P Lou M Kawai C Park DA Egan A Schneider J Bouska R Lesniewski J Henkin, Biochemistry 2003 42 17 5035 5042 10.1021/bi020670c 12718546
24. Small molecule inhibitors of methionine aminopeptidase type 2 (MetAP-2) fail to inhibit endothelial cell proliferation or formation of microvessels from rat aortic rings in vitro. T Garrabrant RW Tuman D Ludovici R Tominovich RL Simoneaux RA Galemmo Jr DL Johnson, Angiogenesis 2004 7 2 91 96 10.1007/s10456-004-6089-7 15516829
25. Metal mediated inhibition of methionine aminopeptidase by quinolinyl sulfonamides. M Huang SX Xie ZQ Ma RP Hanzlik QZ Ye, Biochem Biophys Res Commun 2006 339 2 506 513 10.1016/j.bbrc.2005.11.042 16300729
26. Development of sulfonamide compounds as potent methionine aminopeptidase type II inhibitors with antiproliferative properties. M Kawai NY Bamaung SD Fidanze SA Erickson JS Tedrow WJ Sanders A Vasudevan C Park C Hutchins KM Comess, Bioorg Med Chem Lett 2006 16 13 3574 3577 10.1016/j.bmcl.2006.03.085 16632353
27. Inhibition of Monometalated Methionine Aminopeptidase: Inhibitor Discovery and Crystallographic Analysis. M Huang SX Xie ZQ Ma QQ Huang FJ Nan QZ Ye, J Med Chem 2007
28. Structure of the cobalt-dependent methionine aminopeptidase from Escherichia coli: a new type of proteolytic enzyme. SL Roderick BW Matthews, Biochemistry 1993 32 15 3907 3912 10.1021/bi00066a009 8471602
29. Structure and function of the methionine aminopeptidases. WT Lowther BW Matthews, Biochim Biophys Acta 2000 1477 1-2 157 167 10708856
30. Specificity for inhibitors of metal-substituted methionine aminopeptidase. JY Li LL Chen YM Cui QL Luo J Li FJ Nan QZ Ye, Biochem Biophys Res Commun 2003 307 1 172 179 10.1016/S0006-291X(03)01144-6 12849997
31. The methionyl aminopeptidase from Escherichia coli can function as an iron(II) enzyme. VM D'Souza RC Holz, Biochemistry 1999 38 34 11079 11085 10.1021/bi990872h 10460163
32. Yeast methionine aminopeptidase I can utilize either Zn2+ or Co2+ as a cofactor: a case of mistaken identity? KW Walker RA Bradshaw, Protein Sci 1998 7 12 2684 2687 9865965
33. Structural analysis of metalloform-selective inhibition of methionine aminopeptidase. SX Xie WJ Huang ZQ Ma M Huang RP Hanzlik QZ Ye, Acta Crystallogr D Biol Crystallogr 2006 62 Pt 4 425 432 10.1107/S0907444906003878 16552144
34. Remarks about protein structure precision. DW Cruickshank, Acta Crystallogr D Biol Crystallogr 1999 55 Pt 3 583 601 10.1107/S0907444998012645 10089455
35. Objective comparison of protein structures: error-scaled difference distance matrices. TR Schneider, Acta Crystallogr D Biol Crystallogr 2000 56 Pt 6 714 721 10.1107/S0907444900003723 10818348
36. A genetic algorithm for the identification of conformationally invariant regions in protein molecules. TR Schneider, Acta Crystallogr D Biol Crystallogr 2002 58 Pt 2 195 208 10.1107/S0907444901019291 11807243
37. Characterization of full length and truncated type I human methionine aminopeptidases expressed from Escherichia coli. JY Li LL Chen YM Cui QL Luo M Gu FJ Nan QZ Ye, Biochemistry 2004 43 24 7892 7898 10.1021/bi0360859 15196033
38. Structural basis for the functional differences between type I and type II human methionine aminopeptidases. A Addlagatta X Hu JO Liu BW Matthews, Biochemistry 2005 44 45 14741 14749 10.1021/bi051691k 16274222
39. Structure of the angiogenesis inhibitor ovalicin bound to its noncognate target, human Type 1 methionine aminopeptidase. A Addlagatta BW Matthews, Protein Sci 2006 15 8 1842 1848 10.1110/ps.062278006 16823043
40. Identification of an SH3-binding motif in a new class of methionine aminopeptidases from Mycobacterium tuberculosis suggests a mode of interaction with the ribosome. A Addlagatta ML Quillin O Omotoso JO Liu BW Matthews, Biochemistry 2005 44 19 7166 7174 10.1021/bi0501176 15882055
41. Identification of pyridinylpyrimidines as inhibitors of human methionine aminopeptidases. X Hu A Addlagatta BW Matthews JO Liu, Angew Chem Int Ed Engl 2006 45 23 3772 3775 10.1002/anie.200600757 16724298
42. Elucidation of the function of type 1 human methionine aminopeptidase during cell cycle progression. X Hu A Addlagatta J Lu BW Matthews JO Liu, Proc Natl Acad Sci U S A 2006 103 48 18148 18153 17114291 10.1073/pnas.0608389103
43. Recent changes to the MOSFLM package for processing film and image plate data. AGW Leslie, Joint CCP4 + ESF-EAMCB Newsletter on Protein Crystallography, No 26 1992
44. The CCP4 Suite: Programs for Protein Crystallography. Collaborative Computational Project Number 4, Acta Cryst 1994 D50 760 763
45. A graphical user interface to the CCP4 program suite. E Potterton P Briggs M Turkenburg E Dodson, Acta Crystallogr D Biol Crystallogr 2003 59 Pt 7 1131 1137 10.1107/S0907444903008126 12832755
46. Matthews coefficient probabilities: Improved estimates for unit cell contents of proteins, DNA, and protein-nucleic acid complex crystals. KA Kantardjieff B Rupp, Protein Sci 2003 12 9 1865 1871 10.1110/ps.0350503 12930986
47. MOLREP: an Automated Program for Molecular Replacement. A Vagin A Teplyakov, J Appl Crystallogr 1997 30 1022 1025 10.1107/S0021889897006766
48. Crystallography & NMR system: A new software suite for macromolecular structure determination. AT Brunger PD Adams GM Clore WL DeLano P Gros RW Grosse-Kunstleve JS Jiang J Kuszewski M Nilges NS Pannu, Acta Crystallogr D Biol Crystallogr 1998 54 Pt 5 905 921 10.1107/S0907444998003254 9757107
49. Coot: model-building tools for molecular graphics. P Emsley K Cowtan, Acta Crystallogr D Biol Crystallogr 2004 60 2126 2132 10.1107/S0907444904019158 15572765
50. PROCHECK: a program to check the stereochemical quality of protein structures. RA Laskowski MW MacArthur DS Moss JM Thornton, J Appl Cryst 1993 26 283 291 10.1107/S0021889892009944
51. The PyMOL Molecular Graphics System. WL DeLano, 2002 http://www.pymol.org