The structure of monoacylglycerol lipase from Bacillus sp. H257 reveals unexpected conservation of the cap architecture between bacterial and human enzymes

Biochimica et Biophysica Acta - Molecular and Cell Biology of Lipids

Volumn 1821, Issue 7, 2012, Pages 1012-1021

  Rengachari, Srinivasan ^a   Bezerra, Gustavo A ^a   Riegler Berket, Lina ^a   Gruber, Christian C ^b   Sturm, Christian ^a   Taschler, Ulrike ^a   Boeszoermenyi, Andras ^a   Dreveny, Ingrid ^c   Zimmermann, Robert ^a   Gruber, Karl ^a   Oberer, Monika ^a  

^a UNIVERSITY OF GRAZ   (Austria)

^b AUSTRIAN CENTRE OF INDUSTRIAL BIOTECHNOLOGY   (Austria)

^c UNIVERSITY OF NOTTINGHAM   (United Kingdom)

Author keywords

Evolutionary conservation; Molecular dynamics simulation; Monoacylglycerol lipase; Open conformation; Small angle X ray scattering; X ray crystallography

Indexed keywords

ACYLGLYCEROL LIPASE; ALANINE; ASPARTIC ACID; BENZYLSULFONYL FLUORIDE; HYDROLASE; LYSINE; PROLINE; TYROSINE;

ALPHA HELIX; AMINO ACID SEQUENCE; ARTICLE; BACILLUS; BETA SHEET; CRYSTAL STRUCTURE; ENZYME ACTIVE SITE; ENZYME CONFORMATION; ENZYME STABILITY; ENZYME SUBSTRATE COMPLEX; GENETIC CONSERVATION; HUMAN; HYDROPHOBICITY; MOLECULAR DYNAMICS; NONHUMAN; PRIORITY JOURNAL; PROTEIN STRUCTURE; RADIATION SCATTERING;

AMINO ACID SEQUENCE; BACILLUS; BACTERIAL PROTEINS; CATALYTIC DOMAIN; CLONING, MOLECULAR; CONSERVED SEQUENCE; CRYSTALLOGRAPHY, X-RAY; ESCHERICHIA COLI; HUMANS; HYDROPHOBIC AND HYDROPHILIC INTERACTIONS; MOLECULAR DYNAMICS SIMULATION; MOLECULAR SEQUENCE DATA; MONOACYLGLYCEROL LIPASES; MONOGLYCERIDES; PHENYLMETHYLSULFONYL FLUORIDE; PROTEIN STRUCTURE, SECONDARY; RECOMBINANT PROTEINS; SEQUENCE ALIGNMENT; STRUCTURAL HOMOLOGY, PROTEIN; SUBSTRATE SPECIFICITY;

BACILLUS SP.; BACTERIA (MICROORGANISMS);

EID: 84860826225     PISSN: 13881981     EISSN: 18792618     Source Type: Journal    
DOI: 10.1016/j.bbalip.2012.04.006     Document Type: Article

References (60)

1. H. Tornqvist, and P. Belfrage Purification and some properties of a monoacylglycerol-hydrolyzing enzyme of rat adipose tissue J. Biol. Chem. 251 1976 813 819
2. G. Fredrikson, H. Tornqvist, and P. Belfrage Hormone-sensitive lipase and monoacylglycerol lipase are both required for complete degradation of adipocyte triacylglycerol Biochim. Biophys. Acta 876 1986 288 293
3. T.P. Dinh, S. Kathuria, and D. Piomelli RNA interference suggests a primary role for monoacylglycerol lipase in the degradation of the endocannabinoid 2-arachidonoylglycerol Mol. Pharmacol. 66 2004 1260 1264
4. V. Di Marzo, S.K. Goparaju, L. Wang, J. Liu, S. Batkai, Z. Jarai, F. Fezza, G.I. Miura, R.D. Palmiter, T. Sugiura, and G. Kunos Leptin-regulated endocannabinoids are involved in maintaining food intake Nature 410 2001 822 825
5. A.G. Hohmann, R.L. Suplita, N.M. Bolton, M.H. Neely, D. Fegley, R. Mangieri, J.F. Krey, J.M. Walker, P.V. Holmes, J.D. Crystal, A. Duranti, A. Tontini, M. Mor, G. Tarzia, and D. Piomelli An endocannabinoid mechanism for stress-induced analgesia Nature 435 2005 1108 1112
6. S. Holt, F. Comelli, B. Costa, and C.J. Fowler Inhibitors of fatty acid amide hydrolase reduce carrageenan-induced hind paw inflammation in pentobarbital-treated mice: comparison with indomethacin and possible involvement of cannabinoid receptors Br. J. Pharmacol. 146 2005 467 476
7. G. Marsicano, C.T. Wotjak, S.C. Azad, T. Bisogno, G. Rammes, M.G. Cascio, H. Hermann, J. Tang, C. Hofmann, W. Zieglgansberger, V. Di Marzo, and B. Lutz The endogenous cannabinoid system controls extinction of aversive memories Nature 418 2002 530 534
8. D.K. Nomura, J.Z. Long, S. Niessen, H.S. Hoover, S.W. Ng, and B.F. Cravatt Monoacylglycerol lipase regulates a fatty acid network that promotes cancer pathogenesis Cell 140 2010 49 61
9. L. Ye, B. Zhang, E.G. Seviour, K.X. Tao, X.H. Liu, Y. Ling, J.Y. Chen, and G.B. Wang Monoacylglycerol lipase (MAGL) knockdown inhibits tumor cells growth in colorectal cancer Cancer Lett. 307 2011 6 17
10. V. Di Marzo Targeting the endocannabinoid system: to enhance or reduce? Nat. Rev. Drug Discov. 7 2008 438 455
11. J.Z. Long, W. Li, L. Booker, J.J. Burston, S.G. Kinsey, J.E. Schlosburg, F.J. Pavon, A.M. Serrano, D.E. Selley, L.H. Parsons, A.H. Lichtman, and B.F. Cravatt Selective blockade of 2-arachidonoylglycerol hydrolysis produces cannabinoid behavioral effects Nat. Chem. Biol. 5 2009 37 44
12. A.J. Conley, and J.J. Kabara Antimicrobial action of esters of polyhydric alcohols Antimicrob. Agents Chemother. 4 1973 501 506
13. J.J. Kabara, and R. Vrable Antimicrobial lipids: natural and synthetic fatty acids and monoglycerides Lipids 12 1977 753 759
14. H. Thormar, and H. Hilmarsson The role of microbicidal lipids in host defense against pathogens and their potential as therapeutic agents Chem. Phys. Lipids 150 2007 1 11
15. J.J. Kabara, P. Lynch, K. Krohn, and R. Schemmel The Pharmacological Effect of Lipids 1978 The American Oil Chemists' Society IL 25 36
16. M. Karlsson, H. Tornqvist, and C. Holm Expression, purification, and characterization of histidine-tagged mouse monoglyceride lipase from baculovirus-infected insect cells Protein Expr. Purif. 18 2000 286 292
17. M. Karlsson, J.A. Contreras, U. Hellman, H. Tornqvist, and C. Holm cDNA cloning, tissue distribution, and identification of the catalytic triad of monoglyceride lipase. Evolutionary relationship to esterases, lysophospholipases, and haloperoxidases J. Biol. Chem. 272 1997 27218 27223
18. M. Karlsson, K. Reue, Y.R. Xia, A.J. Lusis, D. Langin, H. Tornqvist, and C. Holm Exon-intron organization and chromosomal localization of the mouse monoglyceride lipase gene Gene 272 2001 11 18
19. T. Sakiyama, T. Yoshimi, A. Miyake, M. Umeoka, A. Tanaka, S. Ozaki, and K. Nakanishi Purification and characterization of a monoacylglycerol lipase from Pseudomonas sp. LP7315 J. Biosci. Bioeng. 91 2001 27 32
20. T. Sakiyama, T. Yoshimi, A. Tanaka, S. Ozaki, and K. Nakanishi Analysis of monoglyceride synthetic reaction in a solvent-free two-phase system catalyzed by a monoacylglycerol lipase from Pseudomonas sp. LP7315 J. Biosci. Bioeng. 91 2001 88 90
21. K. Cotes, R. Dhouib, I. Douchet, H. Chahinian, A. de Caro, F. Carriere, and S. Canaan Characterization of an exported monoglyceride lipase from Mycobacterium tuberculosis possibly involved in the metabolism of host cell membrane lipids Biochem. J. 408 2007 417 427
22. R. Dhouib, F. Laval, F. Carriere, M. Daffe, and S. Canaan A monoacylglycerol lipase from Mycobacterium smegmatis involved in bacterial cell interaction J. Bacteriol. 192 2010 4776 4785
23. S. Imamura, and S. Kitaura Purification and characterization of a monoacylglycerol lipase from the moderately thermophilic Bacillus sp. H-257 J. Biochem. 127 2000 419 425
24. S. Kitaura, K. Suzuki, and S. Imamura Monoacylglycerol lipase from moderately thermophilic Bacillus sp. strain H-257: molecular cloning, sequencing, and expression in Escherichia coli of the gene J. Biochem. 129 2001 397 402
25. C. Heier, U. Taschler, S. Rengachari, M. Oberer, H. Wolinski, K. Natter, S.D. Kohlwein, R. Leber, and R. Zimmermann Identification of Yju3p as functional orthologue of mammalian monoglyceride lipase in the yeast Saccharomyces cerevisiae Biochim. Biophys. Acta 1801 2010 1063 1071
26. S. Imamura, M. Takahasi, H. Misaki, and K. Matsuura Analytical Method Making Use of Monoglyceride Lipase vol. 5162201 1992 Toyo Jozo Co., Ltd. (Shizuoka, JP) United States
27. T. Bertrand, F. Auge, J. Houtmann, A. Rak, F. Vallee, V. Mikol, P.F. Berne, N. Michot, D. Cheuret, C. Hoornaert, and M. Mathieu Structural basis for human monoglyceride lipase inhibition J. Mol. Biol. 396 2010 663 673
28. G. Labar, C. Bauvois, F. Borel, J.L. Ferrer, J. Wouters, and D.M. Lambert Crystal structure of the human monoacylglycerol lipase, a key factor in endocannabinoid signaling Chembiochem 11 2010 218 227
29. C. Schalk-Hihi, C. Schubert, R. Alexander, S. Bayoumy, J.C. Clemente, I. Deckman, R.L. DesJarlais, K.C. Dzordzorme, C.M. Flores, B. Grasberger, J.K. Kranz, F. Lewandowski, L. Liu, H. Ma, D. Maguire, M.J. Macielag, M.E. McDonnell, T. Mezzasalma Haarlander, R. Miller, C. Milligan, C. Reynolds, and L.C. Kuo Crystal structure of a soluble form of human monoglyceride lipase in complex with an inhibitor at 1.35 A resolution Protein Sci. 20 2011 670 683
30. P.V. Konarev, V.V. Volkov, A.V. Sokolova, M.H.J. Koch, and D.I. Svergun PRIMUS: a Windows PC-based system for small-angle scattering data analysis J. Appl. Crystallogr. 36 2003 1277 1282
31. A. Guinier, and G. Fournet Small-angle scattering of X-rays Acta Crystallogr. 9 1956 839
32. A.V. Semenyuk, and D.I. Svergun GNOM - a program package for small-angle scattering data processing J. Appl. Crystallogr. 1991 537 540
33. D.I. Svergun Determination of the regularization parameter in indirect-transform methods using perceptual criteria J. Appl. Crystallogr. 25 1992 495 503
34. D.I. Svergun, C. Barberato, and M.H.J. Koch CRYSOL - a program to evaluate X-ray solution scattering of biological macromolecules from atomic coordinates J. Appl. Crystallogr. 28 1995 768 773
35. A.G.W. Leslie Recent Changes to the MOSFLM Package for Processing Film and Image Plate Data Joint CCP4 + ESF-EAMCB Newsletter on Protein Crystallography No. 26 1992 27 33
36. P. Evans Scaling and assessment of data quality Acta Crystallogr. D Biol. Crystallogr. 62 2006 72 82
37. F. Long, A.A. Vagin, P. Young, and G.N. Murshudov BALBES: a molecular-replacement pipeline Acta Crystallogr. D Biol. Crystallogr. 64 2008 125 132
38. A. Perrakis, R. Morris, and V.S. Lamzin Automated protein model building combined with iterative structure refinement Nat. Struct. Biol. 6 1999 458 463
39. G.N. Murshudov, A.A. Vagin, and E.J. Dodson Refinement of macromolecular structures by the maximum-likelihood method Acta Crystallogr. D Biol. Crystallogr. 53 1997 240 255
40. P.D. Adams, P.V. Afonine, G. Bunkoczi, V.B. Chen, N. Echols, J.J. Headd, L.W. Hung, S. Jain, G.J. Kapral, R.W. Grosse Kunstleve, A.J. McCoy, N.W. Moriarty, R.D. Oeffner, R.J. Read, D.C. Richardson, J.S. Richardson, T.C. Terwilliger, and P.H. Zwart The Phenix software for automated determination of macromolecular structures Methods 55 2011 94 106
41. P. Emsley, and K. Cowtan Coot: model-building tools for molecular graphics Acta Crystallogr. D Biol. Crystallogr. 60 2004 2126 2132
42. V.B. Chen, W.B. Arendall III, J.J. Headd, D.A. Keedy, R.M. Immormino, G.J. Kapral, L.W. Murray, J.S. Richardson, and D.C. Richardson MolProbity: all-atom structure validation for macromolecular crystallography Acta Crystallogr. D Biol. Crystallogr. 66 2010 12 21
43. The PyMOL Molecular Graphics System, Version 1.2r3pre, Schrödinger, LLC. (see also http://www.pymol.org/citing)
44. E. Krieger, G. Koraimann, and G. Vriend Increasing the precision of comparative models with YASARA NOVA - a self-parameterizing force field Proteins 47 2002 393 402
45. M.T. Petersen, P. Martel, E.I. Petersen, F. Drablos, and S.B. Petersen Surface and electrostatics of cutinases Methods Enzymol. 284 1997 130 154
46. B. Hess, B. Kutzner, D. van der Spoel, and E. Lindahl GROMACS 4: algorithms for highly efficient, load-balanced, and scalable molecular simulation J. Chem. Theory Comput. 4 2008 435 447
47. G.A. Kaminski, R.A. Friesner, J. Tirado-Rives, and W.L. Jorgensen Evaluation and reparametrization of the OPLS-AA force field for proteins via comparison with accurate quantum chemical calculations on peptides J. Phys. Chem. B 105 2001 6474 6487
48. D.J. Price, and C.L. Brooks III A modified TIP3P water potential for simulation with Ewald summation J. Chem. Phys. 121 2004 10096 10103
49. M. Petrek, P. Kosinova, J. Koca, and M. Otyepka MOLE: a Voronoi diagram-based explorer of molecular channels, pores, and tunnels Structure 15 2007 1357 1363
50. P.D. Carr, and D.L. Ollis Alpha/beta hydrolase fold: an update Protein Pept. Lett. 16 2009 1137 1148
51. G. van Pouderoyen, T. Eggert, K.E. Jaeger, and B.W. Dijkstra The crystal structure of Bacillus subtilis lipase: a minimal alpha/beta hydrolase fold enzyme J. Mol. Biol. 309 2001 215 226
52. G. Steinkellner, R. Rader, G.G. Thallinger, C. Kratky, and K. Gruber VASCo: computation and visualization of annotated protein surface contacts BMC Bioinformatics 10 2009 32
53. S. Rehm, P. Trodler, and J. Pleiss Solvent-induced lid opening in lipases: a molecular dynamics study Protein Sci. 19 2010 2122 2130
54. A.R. King, A. Lodola, C. Carmi, J. Fu, M. Mor, and D. Piomelli A critical cysteine residue in monoacylglycerol lipase is targeted by a new class of isothiazolinone-based enzyme inhibitors Br. J. Pharmacol. 157 2009 974 983
55. S. Chakravarty, and R. Varadarajan Elucidation of factors responsible for enhanced thermal stability of proteins: a structural genomics based study Biochemistry 41 2002 8152 8161
56. J.N. Sarakatsannis, and Y. Duan Statistical characterization of salt bridges in proteins Proteins 60 2005 732 739
57. J.P. Gallivan, and D.A. Dougherty Cation-π interactions in structural biology Proc. Natl. Acad. Sci. U. S. A. 96 1999 9459 9464
58. L. Holm, and P. Rosenstrom Dali server: conservation mapping in 3D Nucleic Acids Res. 38 2010 W545 W549
59. D.C. Goldstone, S.G. Villas-Boas, M. Till, W.J. Kelly, G.T. Attwood, and V.L. Arcus Structural and functional characterization of a promiscuous feruloyl esterase (Est1E) from the rumen bacterium Butyrivibrio proteoclasticus Proteins 78 2010 1457 1469
60. A.C. Wallace, R.A. Laskowski, and J.M. Thornton LIGPLOT: a program to generate schematic diagrams of protein-ligand interactions Protein Eng. 8 1995 127 134