A novel family of soluble minimal scaffolds provides structural insight into the catalytic domains of integral membrane metallopeptidases

Journal of Biological Chemistry

Volumn 288, Issue 29, 2013, Pages 21279-21294

  López Pelegrín, Mar ^a   Cerdà Costa, Núria ^a   Martínez Jiménez, Francisco ^b,c   Cintas Pedrola, Anna ^a   Canals, Albert ^d   Peinado, Juan R ^a,f   Marti Renom, Marc A ^c,d   López Otín, Carlos ^e   Arolas, Joan L ^a   Gomis Rüth, F Xavier ^a  

^a INSTITUT DE BIOLOGIA MOLECULAR DE BARCELONA   (Spain)

^b Centre Nacional d'Analisi Genomica   (Spain)

^c CENTRE FOR GENOMIC REGULATION CRG   (Spain)

^d INSTITUTE FOR RESEARCH IN BIOMEDICINE   (Spain)

^e DEPARTAMENTO DE BIOQUÍMICA Y BIOLOGÍA MOLECULAR   (Spain)

^f UNIVERSITY OF CASTILLA LA MANCHA   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

CATALYTIC DOMAINS; HIGH RESOLUTION; INTEGRAL MEMBRANE; METALLOPEPTIDASES; SMALL MOLECULE INHIBITOR; STRUCTURAL CHARACTERIZATION; STRUCTURAL INSIGHTS;

BIOCHEMISTRY; BIOLOGY;

SCAFFOLDS;

ADENOSINE TRIPHOSPHATE; DOUBLE STRANDED DNA; ENZYME PRECURSOR; LEUKOTRIENE A4 HYDROLASE; METALLOPROTEINASE; THERMOLYSIN;

AMINO ACID SEQUENCE; ARTICLE; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME ACTIVE SITE; ENZYME SYNTHESIS; GENE INSERTION; GENE OVEREXPRESSION; GENETIC ASSOCIATION; METHANOCALDOCOCCUS JANNASCHII; MOLECULAR CLONING; NONHUMAN; PRIORITY JOURNAL; PROKARYOTE; PROTEIN ANALYSIS; PROTEIN DEGRADATION; PROTEIN STRUCTURE; PYROCOCCUS ABYSSI;

CATALYTIC DOMAIN; ENZYME MECHANISMS; ENZYME STRUCTURE; ENZYMOLOGY; MEMBRANE ENZYMES; METALLOPEPTIDASE; METALLOPROTEASE; MOLECULAR MODEL; MOLECULAR MODELING; ZYMOGEN;

AMINO ACID SEQUENCE; ARCHAEA; ARCHAEAL PROTEINS; CATALYTIC DOMAIN; COMPUTATIONAL BIOLOGY; CRYSTALLOGRAPHY, X-RAY; ENZYME ACTIVATION; ENZYME ASSAYS; ENZYME PRECURSORS; HUMANS; MEMBRANE PROTEINS; METALLOPROTEASES; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PROTEOLYSIS; PYROCOCCUS; SOLUBILITY; STRUCTURAL HOMOLOGY, PROTEIN;

EID: 84880520015     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.476580     Document Type: Article

References (101)

1. Wallin, E., and von Heijne, G. (1998) Genome-wide analysis of integral membrane proteins from eubacterial, archaean, and eukaryotic organisms. Protein Sci. 7, 1029-1038
2. Sonoda, Y., Newstead, S., Hu, N. J., Alguel, Y., Nji, E., Beis, K., Yashiro, S., Lee, C., Leung, J., Cameron, A. D., Byrne, B., Iwata, S., and Drew, D. (2011) Benchmarking membrane protein detergent stability for improving throughput of high resolution x-ray structures. Structure 19, 17-25
3. Almén, M. S., Nordström, K. J., Fredriksson, R., and Schiöth, H. B. (2009) Mapping the human membrane proteome: a majority of the human membrane proteins can be classified according to function and evolutionary origin. BMC Biol. 7, 50
4. Kim, H., Melén, K., Osterberg, M., and von Heijne, G. (2006) A global topology map of the Saccharomyces cerevisiae membrane proteome. Proc. Natl. Acad. Sci. U.S.A. 103, 11142-11147
5. Terstappen, G. C., and Reggiani, A. (2001) In silico research in drug discovery. Trends Pharmacol. Sci. 22, 23-26
6. Davey, J. (2004) G-protein-coupled receptors: new approaches to maximise the impact of GPCRS in drug discovery. Expert Opin. Ther. Targets 8, 165-170
7. Rawlings, N. D., Barrett, A. J., and Bateman, A. (2012) MEROPS: the database of proteolytic enzymes, their substrates and inhibitors. Nucleic Acids Res. 40, D343-D350
8. Tusnády, G. E., Dosztányi, Z., and Simon, I. (2004) Transmembrane proteins in the Protein Data Bank: identification and classification. Bioinformatics 20, 2964-2972
9. Fujimura-Kamada, K., Nouvet, F. J., and Michaelis, S. (1997) A novel membrane-associated metalloprotease, Ste24p, is required for the first step of NH2-terminal processing of the yeast α-factor precursor. J. Cell Biol. 136, 271-285
10. Freije, J. M., Blay, P., Pendás, A. M., Cadiñanos, J., Crespo, P., and López-Otín, C. (1999) Identification and chromosomal location of two human genes encoding enzymes potentially involved in proteolytic maturation of farnesylated proteins. Genomics 58, 270-280
11. Barrowman, J., and Michaelis, S. (2009) ZMPSTE24, an integral membrane zinc metalloprotease with a connection to progeroid disorders. Biol. Chem. 390, 761-773
12. Varela, I., Pereira, S., Ugalde, A. P., Navarro, C. L., Suárez, M. F., Cau, P., Cadiñanos, J., Osorio, F. G., Foray, N., Cobo, J., de Carlos, F., Lévy, N., Freije, J. M., and López-Otín, C. (2008) Combined treatment with statins and aminobisphosphonates extends longevity in a mouse model of human premature aging. Nat. Med. 14, 767-772
13. Freije, J. M., and López-Otín, C. (2012) Reprogramming aging and progeria. Curr. Opin. Cell Biol. 24, 757-764
14. Akiyama, Y. (2009) Quality control of cytoplasmic membrane proteins in Escherichia coli. J. Biochem. 146, 449-454
15. Bieniossek, C., Schalch, T., Bumann, M., Meister, M., Meier, R., and Baumann, U. (2006) The molecular architecture of the metalloprotease FtsH. Proc. Natl. Acad. Sci. U.S.A. 103, 3066-3071
16. Sakoh, M., Ito, K., and Akiyama, Y. (2005) Proteolytic activity of HtpX, a membrane-bound and stress-controlled protease from Escherichia coli. J. Biol. Chem. 280, 33305-33310
17. Suno, R., Niwa, H., Tsuchiya, D., Zhang, X., Yoshida, M., and Morikawa, K. (2006) Structure of the whole cytosolic region of ATP-dependent protease FtsH. Mol. Cell 22, 575-585
18. Kaser, M., Kambacheld, M., Kisters-Woike, B., and Langer, T. (2003) Oma1, a novel membrane-bound metallopeptidase in mitochondria with activities overlapping with the m-AAA protease. J. Biol. Chem. 278, 46414-46423
19. McBride, H., and Soubannier, V. (2010) Mitochondrial function: OMA1 and OPA1, the grandmasters of mitochondrial health. Curr. Biol. 20, R274-R276
20. Quirós, P. M., Ramsay, A. J., Sala, D., Fernández-Vizarra, E., Rodríguez, F., Peinado, J. R., Fernández-García, M. S., Vega, J. A., Enríquez, J. A., Zorzano, A., and López-Otín, C. (2012) Loss of mitochondrial protease OMA1 alters processing of the GTPase OPA1 and causes obesity and defective thermogenesis in mice. EMBO J. 31, 2117-2133
21. Mallorquí-Fernández, G., Marrero, A., García- Piquè, S., García-Castellanos, R., and Gomis-Rüth, F. X. (2004) Staphylococcal methicillin resistance: fine focus on folds and functions. FEMS Microbiol. Lett. 235, 1-8
22. Fuda, C. C., Fisher, J. F., and Mobashery, S. (2005) β-Lactam resistance in Staphylococcus aureus: the adaptive resistance of a plastic genome. Cell. Mol. Life Sci. 62, 2617-2633
23. Llarrull, L. I., Testero, S. A., Fisher, J. F., and Mobashery, S. (2010) The future of the β-lactams. Curr. Opin. Microbiol. 13, 551-557
24. Llarrull, L. I., and Mobashery, S. (2012) Dissection of events in the resistance to β-lactam antibiotics mediated by the protein BlaR1 from. Staphylococcus aureus. Biochemistry 51, 4642-4649
25. Zhu, Y., Englebert, S., Joris, B., Ghuysen, J. M., Kobayashi, T., and Lampen, J. O. (1992) Structure, function, and fate of the BlaR signal transducer involved in induction of β-lactamase in Bacillus licheniformis. J. Bacteriol. 174, 6171-6178
26. Hardt, K., Joris, B., Lepage, S., Brasseur, R., Lampen, J. O., Frère, J. M., Fink, A. L., and Ghuysen, J. M. (1997) The penicillin sensory transducer, BlaR, involved in the inducibility of β-lactamase synthesis in Bacillus licheniformis is embedded in the plasma membrane via a four-α-helix bundle. Mol. Microbiol. 23, 935-944
27. Berzigotti, S., Benlafya, K., Sépulchre, J., Amoroso, A., and Joris, B. (2012) Bacillus licheniformis BlaR1 L3 loop is a zinc metalloprotease activated by self-proteolysis. PLoS ONE 7, e36400
28. Hao, H., Dai, M., Wang, Y., Huang, L., and Yuan, Z. (2012) Key genetic elements and regulation systems in methicillin-resistant Staphylococcus aureus. Future Microbiol. 7, 1315-1329
29. Marrero, A., Mallorquí-Fernández, G., Guevara, T., García-Castellanos, R., and Gomis-Rüth, F. X. (2006) Unbound and acylated structures of the MecR1 extracellular antibiotic-sensor domain provide insights into the signal-transduction system that triggers methicillin resistance. J. Mol. Biol. 361, 506-521
30. Birck, C., Cha, J. Y., Cross, J., Schulze-Briese, C., Meroueh, S. O., Schlegel, H. B., Mobashery, S., and Samama, J.-P. (2004) X-ray crystal structure of the acylated β-lactam sensor domain of BlaR1 from Staphylococcus aureus and the mechanism of receptor activation for signal transduction. J. Am. Chem. Soc. 126, 13945-13947
31. Wilke, M. S., Hills, T. L., Zhang, H. Z., Chambers, H. F., and Strynadka, N. C. (2004) Crystal structures of the apo and penicillin-acylated forms of the BlaR1 β-lactam sensor of Staphylococcus aureus. J. Biol. Chem. 279, 47278-47287
32. Kerff, F., Charlier, P., Colombo, M.-L., Sauvage, E., Brans, A., Frère, J.-M., Joris, B., and Fonzé, E. (2003) Crystal structure of the sensor domain of the BlaR penicillin receptor from Bacillus licheniformis. Biochemistry 42, 12835-12843
33. Kuntz, I. D. (1992) Structure-based strategies for drug design and discovery. Science 257, 1078-1082
34. Greer, J., Erickson, J. W., Baldwin, J. J., and Varney, M. D. (1994) Application of the three-dimensional structures of protein target molecules in structure-based drug design. J. Med. Chem. 37, 1035-1054
35. Arinaminpathy, Y., Khurana, E., Engelman, D. M., and Gerstein, M. B. (2009) Computational analysis of membrane proteins: the largest class of drug targets. Drug Discov. Today 14, 1130-1135
36. Feng, L., Yan, H., Wu, Z., Yan, N., Wang, Z., Jeffrey, P. D., and Shi, Y. (2007) Structure of a site-2 protease family intramembrane metalloprotease. Science 318, 1608-1612
37. Wolfe, M. S. (2009) Intramembrane proteolysis. Chem. Rev. 109, 1599-1612
38. Wolfe, M. S. (2009) Intramembrane-cleaving proteases. J. Biol. Chem. 284, 13969-13973
39. Pryor, E. E., Jr., Horanyi, P. S., Clark, K. M., Fedoriw, N., Connelly, S. M., Koszelak-Rosenblum, M., Zhu, G., Malkowski, M. G., Wiener, M. C., and Dumont, M. E. (2013) Structure of the integral membrane protein CAAX protease Ste24p. Science 339, 1600-1604
40. Quigley, A., Dong, Y. Y., Pike, A. C., Dong, L., Shrestha, L., Berridge, G., Stansfeld, P. J., Sansom, M. S., Edwards, A. M., Bountra, C., von Delft, F., Bullock, A. N., Burgess-Brown, N. A., and Carpenter, E. P. (2013) The structural basis of ZMPSTE24-dependent laminopathies. Science 339, 1604-1607
41. Bode, W., Gomis-Rüth, F. X., and Stöckler, W. (1993) Astacins, serralysins, snake venom, and matrix metalloproteinases exhibit identical zinc-binding environments (HEXXHXXGXXH and Met-turn) and topologies and should be grouped into a common family, the 'metzincins'. FEBS Lett. 331, 134-140
42. Hooper, N. M. (1994) Families of zinc metalloproteases. FEBS Lett. 354, 1-6
43. McKerrow, J. H. (1987) Human fibroblast collagenase contains an amino acid sequence homologous to the zinc-binding site of Serratia protease. J. Biol. Chem. 262, 5943-5943
44. Gomis-Rüth, F. X., Botelho, T. O., and Bode, W. (2012) A standard orientation for metallopeptidases. Biochim. Biophys. Acta 1824, 157-163
45. Altschul, S. F., Madden, T. L., Schäffer, A. A., Zhang, J., Zhang, Z., Miller, W., and Lipman, D. J. (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 25, 3389-3402
46. Sánchez, R., Serra, F., Tárraga, J., Medina, I., Carbonell, J., Pulido, L., de María, A., Capella-Gutíerrez, S., Huerta-Cepas, J., Gabaldón, T., Dopazo, J., and Dopazo, H. (2011) Phylemon 2.0: a suite of web-tools for molecular evolution, phylogenetics, phylogenomics, and hypotheses testing. Nucleic Acids Res. 39, W470-W474
47. Capella-Gutiérrez, S., Silla-Martínez, J. M., and Gabaldón, T. (2009) TrimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses. Bioinformatics 25, 1972-1973
48. Darriba, D., Taboada, G. L., Doallo, R., and Posada, D. (2011) ProtTest 3: fast selection of best-fit models of protein evolution. Bioinformatics 27, 1164-1165
49. Guindon, S., and Gascuel, O. (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst. Biol. 52, 696-704
50. Cole, C., Barber, J. D., and Barton, G. J. (2008) The Jpred 3 secondary structure prediction server. Nucleic Acids Res. 36, W197-W201
51. Tallant, C., García-Castellanos, R., Baumann, U., and Gomis-Rüth, F. X. (2010) On the relevance of the Met-turn methionine in metzincins. J. Biol. Chem. 285, 13951-13957
52. Goulas, T., Arolas, J. L., and Gomis-Rüth, F. X. (2011) Structure, function, and latency regulation of a bacterial enterotoxin potentially derived from a mammalian adamalysin/ADAM xenolog. Proc. Natl. Acad. Sci. U.S.A. 108, 1856-1861
53. Tallant, C., García-Castellanos, R., Seco, J., Baumann, U., and Gomis-Rüth, F. X. (2006) Molecular analysis of ulilysin, the structural prototype of a new family of metzincin metalloproteases. J. Biol. Chem. 281, 17920-17928
54. Botelho, T. O., Guevara, T., Marrero, A., Arêde, P., Fluxà, V. S., Reymond, J. L., Oliveira, D. C., and Gomis-Rüth, F. X. (2011) Structural and functional analyses reveal that Staphylococcus aureus antibiotic resistance factor HmrA is a zinc-dependent endopeptidase. J. Biol. Chem. 286, 25697-25709
55. Kabsch, W. (2010) XDS. Acta Crystallogr. D Biol. Crystallogr. 66, 125-132
56. Kabsch, W. (2010) Integration, scaling, space-group assignment and post-refinement. Acta Crystallogr. D Biol. Crystallogr. 66, 133-144
57. Evans, P. R. (2011) An introduction to data reduction: space-group determination, scaling and intensity statistics. Acta Crystallogr. D Biol. Crystallogr. 67, 282-292
58. Winn, M. D., Ballard, C. C., Cowtan, K. D., Dodson, E. J., Emsley, P., Evans, P. R., Keegan, R. M., Krissinel, E. B., Leslie, A. G., McCoy, A., McNicholas, S. J., Murshudov, G. N., Pannu, N. S., Potterton, E. A., Powell, H. R., Read, R. J., Vagin, A., and Wilson, K. S. (2011) Overview of the CCP4 suite and current developments. Acta Crystallogr. D Biol. Crystallogr. 67, 235-242
59. Sheldrick, G. M. (2010) Experimental phasing with SHELXC/D/E: combining chain tracing with density modification. Acta Crystallogr. D Biol. Crystallogr. 66, 479-485
60. Sheldrick, G. M. (2011) The SHELX approach to experimental phasing of macromolecules. Acta Crystallogr. Sect. A 67, C13
61. Hübschle, C. B., Dittrich, B., and Sheldrick, G. M. (2012) SHELXE-a GUI for SHELXL. Acta Crystallogr. Sect. A 68, s121
62. Carranza, C., Inisan, A.-G., Mouthuy-Knoops, E., Cambillau, C., and Roussel, A. (1999) AFMB Activity Report 1996-1999, pp. 89-90, CNRSUPR 9039, Marseille
63. Debreczeni, J. É., and Emsley, P. (2012) Handling ligands with Coot. Acta Crystallogr. D Biol. Crystallogr. 68, 425-430
64. Emsley, P., Lohkamp, B., Scott, W. G., and Cowtan, K. (2010) Features and development of Coot. Acta Crystallogr. D Biol. Crystallogr. 66, 486-501
65. Smart, O. S., Womack, T. O., Flensburg, C., Keller, P., Paciorek, W., Sharff, A., Vonrhein, C., and Bricogne, G. (2012) Exploiting structure similarity in refinement: automated NCS and target-structure restraints in BUSTER. Acta Crystallogr. D Biol. Crystallogr. 68, 368-380
66. Cowtan, K. (2010) Recent developments in classical density modification. Acta Crystallogr. D Biol. Crystallogr. 66, 470-478
67. Pettersen, E. F., Goddard, T. D., Huang, C. C., Couch, G. S., Greenblatt, D. M., Meng, E. C., and Ferrin, T. E. (2004) UCSF Chimera-a visualization system for exploratory research and analysis. J. Comput. Chem. 25, 1605-1612
68. Brünger, A. T., Adams, P. D., Clore, G. M., DeLano, W. L., Gros, P., Grosse-Kunstleve, R. W., Jiang, J.-S., Kuszewski, J., Nilges, M., Pannu, N. S., Read, R. J., Rice, L. M., Simonson, T., and Warren, G. L. (1998) Crystallography & NMR system: a new software suite for macromolecular structure determination. Acta Crystallogr. D Biol. Crystallogr. 54, 905-921
69. Krissinel, E., and Henrick, K. (2004) Secondary-structure matching (SSM), a new tool for fast protein structure alignment in three dimensions. Acta Crystallogr. D Biol. Crystallogr. 60, 2256-2268
70. Lawrence, M. C., and Colman, P. M. (1993) Shape complementarity at protein/protein interfaces. J. Mol. Biol. 234, 946-950
71. Chen, V. B., Arendall, W. B., 3rd, Headd, J. J., Keedy, D. A., Immormino, R. M., Kapral, G. J., Murray, L. W., Richardson, J. S., and Richardson, D. C. (2010) MolProbity: all-atom structure validation for macromolecular crystallography. Acta Crystallogr. D Biol. Crystallogr. 66, 12-21
72. Vriend, G. (1990) What if: a molecular modelling and drug design program. J. Mol. Graph. 8, 52-56
73. Ortiz, A. R., Strauss, C. E., and Olmea, O. (2002)MAMMOTH(matching molecular models obtained from theory): an automated method for model comparison. Protein Sci. 11, 2606-2621
74. Berman, H. M., Battistuz, T., Bhat, T. N., Bluhm, W. F., Bourne, P. E., Burkhardt, K., Feng, Z., Gilliland, G. L., Iype, L., Jain, S., Fagan, P., Marvin, J., Padilla, D., Ravichandran, V., Schneider, B., Thanki, N., Weissig, H., Westbrook, J. D., and Zardecki, C. (2002) The Protein Data Bank. Acta Crystallogr. D Biol. Crystallogr. 58, 899-907
75. Holm, L., and Rosenström, P. (2010) Dali server: conservation mapping in 3D. Nucleic Acids Res. 38, W545-W549
76. Schechter, I., and Berger, A. (1967) On the size of active site in proteases. I. Papain. Biochem. Biophys. Res. Commun. 27, 157-162
77. Tallant, C., Marrero, A., and Gomis-Rüth, F. X. (2010) Matrix metalloproteinases: fold and function of their catalytic domains. Biochim. Biophys. Acta 1803, 20-28
78. Takeda, S. (2009) Three-dimensional domain architecture of theADAM family proteinases. Semin. Cell Dev. Biol. 20, 146-152
79. Takeda, S., Takeya, H., and Iwanaga, S. (2012) Snake venom metalloproteinases: Structure, function, and relevance to the mammalian ADAM/ ADAMTS family proteins. Biochim. Biophys. Acta 1824, 164-176
80. Guevara, T., Yiallouros, I., Kappelhoff, R., Bissdorf, S., Stöcker, W., and Gomis-Rüth, F. X. (2010) Proenzyme structure and activation of astacin metallopeptidase. J. Biol. Chem. 285, 13958-13965
81. Arolas, J. L., Broder, C., Jefferson, T., Guevara, T., Sterchi, E. E., Bode, W., Stöcker, W., Becker-Pauly, C., and Gomis-Rüth, F. X. (2012) Structural basis for the sheddase function of human meprin β- metalloproteinase at the plasma membrane. Proc. Natl. Acad. Sci. U.S.A. 109, 16131-16136
82. Gomis-Rüth, F. X. (2008) Structure and mechanism of metallocarboxypeptidases. Crit. Rev. Biochem. Mol. Biol. 43, 319-345
83. Gao, X., Wang, J., Yu, D. Q., Bian, F., Xie, B. B., Chen, X. L., Zhou, B. C., Lai, L. H., Wang, Z. X., Wu, J. W., and Zhang, Y. Z. (2010) Structural basis for the autoprocessing of zinc metalloproteases in the thermolysin family. Proc. Natl. Acad. Sci. U.S.A. 107, 17569-17574
84. Janin, J., and Chothia, C. (1990) The structure of protein-protein recognition sites. J. Biol. Chem. 265, 16027-16030
85. Harding, M. M. (2004) The architecture of metal coordination groups in proteins. Acta Crystallogr. D Biol. Crystallogr. 60, 849-859
86. Matthews, B. W., Jansonius, J. N., Colman, P. M., Schoenborn, B. P., and Dupourque, D. (1972) Three-dimensional structure of thermolysin. Nat. New Biol. 238, 37-41
87. Tholander, F., Muroya, A., Roques, B. P., Fournié-Zaluski, M. C., Thunnissen, M. M., and Haeggström, J. Z. (2008) Structure-based dissection of the active site chemistry of leukotriene A4 hydrolase: implications forM1 aminopeptidases and inhibitor design. Chem. Biol. 15, 920-929
88. Bauvois, C., Jacquamet, L., Huston, A. L., Borel, F., Feller, G., and Ferrer, J. L. (2008) Crystal structure of the cold-active aminopeptidase from Colwellia psychrerythraea, a close structural homologue of the human bifunctional leukotriene A4 hydrolase. J. Biol. Chem. 283, 23315-23325
89. Nguyen, T. T., Chang, S. C., Evnouchidou, I., York, I. A., Zikos, C., Rock, K. L., Goldberg, A. L., Stratikos, E., and Stern, L. J. (2011) Structural basis for antigenic peptide precursor processing by the endoplasmic reticulum aminopeptidase ERAP1. Nat. Struct. Mol. Biol. 18, 604-613
90. Kochan, G., Krojer, T., Harvey, D., Fischer, R., Chen, L., Vollmar, M., von Delft, F., Kavanagh, K. L., Brown, M. A., Bowness, P., Wordsworth, P., Kessler, B. M., and Oppermann, U. (2011) Crystal structures of the endoplasmic reticulum aminopeptidase-1 (ERAP1) reveal the molecular basis for N-terminal peptide trimming. Proc. Natl. Acad. Sci. U.S.A. 108, 7745-7750
91. Kyrieleis, O. J., Goettig, P., Kiefersauer, R., Huber, R., and Brandstetter, H. (2005) Crystal structures of the tricorn interacting factor F3 from Thermoplasma acidophilum, a zinc aminopeptidase in three different conformations. J. Mol. Biol. 349, 787-800
92. McGowan, S., Porter, C. J., Lowther, J., Stack, C. M., Golding, S. J., Skinner-Adams, T. S., Trenholme, K. R., Teuscher, F., Donnelly, S. M., Grembecka, J., Mucha, A., Kafarski, P., Degori, R., Buckle, A. M., Gardiner, D. L., Whisstock, J. C., and Dalton, J. P. (2009) Structural basis for the inhibition of the essential Plasmodium falciparum M1 neutral aminopeptidase. Proc. Natl. Acad. Sci. U.S.A. 106, 2537-2542
93. Addlagatta, A., Gay, L., and Matthews, B. W. (2006) Structure of aminopeptidase N from Escherichia coli suggests a compartmentalized, gated active site. Proc. Natl. Acad. Sci. U.S.A. 103, 13339-13344
94. Gomis-Rüth, F. X. (2003) Structural aspects of the metzincin clan of metalloendopeptidases. Mol. Biotechnol. 24, 157-202
95. Zhan, C., Fedorov, E. V., Shi, W., Ramagopal, U. A., Thirumuruhan, R., Manjasetty, B. A., Almo, S. C., Fiser, A., Chance, M. R., and Fedorov, A. A. (2005) The ybeY protein from Escherichia coli is a metalloprotein. Acta Crystallogr. Sect. F Struct. Biol. Cryst. Commun. 61, 959-963
96. Oganesyan, V., Busso, D., Brandsen, J., Chen, S., Jancarik, J., Kim, R., and Kim, S. H. (2003) Structure of the hypothetical protein AQ-1354 from Aquifex aeolicus. Acta Crystallogr. D Biol. Crystallogr. 59, 1219-1223
97. Weiss, M. S. (2001) Global indicators of x-ray quality. J. Appl. Cryst. 34, 130-135
98. Evans, P. (2006) Scaling and assessment of data quality. Acta Crystallogr. D Biol. Crystallogr. 62, 72-82
99. Bernsel, A., Viklund, H., Hennerdal, A., and Elofsson, A. (2009) TOPCONS: consensus prediction of membrane protein topology. Nucleic Acids Res. 37, W465-W468
100. Corpet, F. (1988) Multiple sequence alignment with hierarchical clustering. Nucleic Acids Res. 16, 10881-10890
101. Holmes, M. A., and Matthews, B. W. (1981) Binding of hydroxamic acid inhibitors to crystalline thermolysin suggests a pentacoordinate zinc intermediate in catalysis. Biochemistry 20, 6912-6920