Structure and mechanism of Escherichia coli type I signal peptidase

Biochimica et Biophysica Acta - Molecular Cell Research

Volumn 1843, Issue 8, 2014, Pages 1497-1508

  Paetzel, Mark ^a  

^a SIMON FRASER UNIVERSITY   (Canada)

Author keywords

Leader peptidase; Leader peptide; Preprotein processing; Protein secretion; Signal peptidase; Signal peptide

Indexed keywords

ESCHERICHIA COLI TYPE I SIGNAL PEPTIDASE; SIGNAL PEPTIDASE; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; BACTERIAL MEMBRANE; CROSS LINKING; CRYSTAL STRUCTURE; DEACYLATION; DISULFIDE BOND; DNA SEQUENCE; ENZYME ACTIVE SITE; ENZYME DEGRADATION; ENZYME KINETICS; ENZYME MECHANISM; ENZYME PURIFICATION; ENZYME STRUCTURE; HYDROGEN BOND; IC 50; IN VITRO STUDY; IN VIVO STUDY; MEMBRANE STRUCTURE; MOLECULAR RECOGNITION; MOLECULAR WEIGHT; NONHUMAN; PRIORITY JOURNAL; PROTEIN SECRETION; REVIEW; SEQUENCE ALIGNMENT; SITE DIRECTED MUTAGENESIS;

LEADER PEPTIDASE; LEADER PEPTIDE; PREPROTEIN PROCESSING; PROTEIN SECRETION; SIGNAL PEPTIDASE; SIGNAL PEPTIDE;

BINDING SITES; CELL MEMBRANE; ESCHERICHIA COLI; MEMBRANE PROTEINS; PROTEIN CONFORMATION; PROTEIN SORTING SIGNALS; PROTEIN TRANSPORT; SERINE ENDOPEPTIDASES;

EID: 84902299780     PISSN: 01674889     EISSN: 18792596     Source Type: Journal    
DOI: 10.1016/j.bbamcr.2013.12.003     Document Type: Review

References (123)

1. Chatzi K.E., Sardis M.F., Karamanou S., Economou A. Breaking on through to the other side: protein export through the bacterial Sec system. Biochem. J. 2013, 449:25-37.
2. Driessen A.J., Nouwen N. Protein translocation across the bacterial cytoplasmic membrane. Annu. Rev. Biochem. 2008, 77:643-667.
3. Chimalapati S., Sankaran K., Brown J.S. Chapter 62 - signal peptidase II. Handbook of Proteolytic Enzymes 2013, 258-261. Academic Press.
4. Dupuy B., Deghmane A.-E., Taha M.-K. Chapter 63 - type IV prepilin peptidase. Handbook of Proteolytic Enzymes 2013, 261-265. Academic Press.
5. von Heijne G. The signal peptide. J. Membr. Biol. 1990, 115:195-201.
6. von Heijne G. Signal sequences. The limits of variation. J. Mol. Biol. 1985, 184:99-105.
7. von Heijne G. Patterns of amino acids near signal-sequence cleavage sites. Eur. J. Biochem. 1983, 133:17-21.
8. Perlman D., Halvorson H.O. A putative signal peptidase recognition site and sequence in eukaryotic and prokaryotic signal peptides. J. Mol. Biol. 1983, 167:391-409.
9. Nielsen H., Engelbrecht J., Brunak S., von Heijne G. A neural network method for identification of prokaryotic and eukaryotic signal peptides and prediction of their cleavage sites. Int. J. Neural Syst. 1997, 8:581-599.
10. Nielsen H., Engelbrecht J., Brunak S., von Heijne G. Identification of prokaryotic and eukaryotic signal peptides and prediction of their cleavage sites. Protein Eng. 1997, 10:1-6.
11. UniProt C. Update on activities at the Universal Protein Resource (UniProt) in 2013. Nucleic Acids Res. 2013, 41:D43-D47.
12. Apweiler R., Bairoch A., Wu C.H., Barker W.C., Boeckmann B., Ferro S., Gasteiger E., Huang H., Lopez R., Magrane M., Martin M.J., Natale D.A., O'Donovan C., Redaschi N., Yeh L.S. UniProt: the Universal Protein knowledgebase. Nucleic Acids Res. 2004, 32:D115-D119.
13. Bendtsen J.D., Nielsen H., von Heijne G., Brunak S. Improved prediction of signal peptides: SignalP 3.0. J. Mol. Biol. 2004, 340:783-795.
14. Petersen T.N., Brunak S., von Heijne G., Nielsen H. SignalP 4.0: discriminating signal peptides from transmembrane regions. Nat. Methods 2011, 8:785-786.
15. Ivankov D.N., Payne S.H., Galperin M.Y., Bonissone S., Pevzner P.A., Frishman D. How many signal peptides are there in bacteria?. Environ. Microbiol. 2013, 15:983-990.
16. Choo K.H., Tan T.W., Ranganathan S. SPdb-a signal peptide database. BMC Bioinforma. 2005, 6:249.
17. Rudd K.E. EcoGene: a genome sequence database for Escherichia coli K-12. Nucleic Acids Res. 2000, 28:60-64.
18. Zhou J., Rudd K.E. EcoGene 3.0. Nucleic Acids Res. 2013, 41:D613-D624.
19. Dev I.K., Ray P.H., Novak P. Minimum substrate sequence for signal peptidase I of Escherichia coli. J. Biol. Chem. 1990, 265:20069-20072.
20. Shen L.M., Lee J.I., Cheng S.Y., Jutte H., Kuhn A., Dalbey R.E. Use of site-directed mutagenesis to define the limits of sequence variation tolerated for processing of the M13 procoat protein by the Escherichia coli leader peptidase. Biochemistry 1991, 30:11775-11781.
21. Karamyshev A.L., Karamysheva Z.N., Kajava A.V., Ksenzenko V.N., Nesmeyanova M.A. Processing of Escherichia coli alkaline phosphatase: role of the primary structure of the signal peptide cleavage region. J. Mol. Biol. 1998, 277:859-870.
22. Kajava A.V., Zolov S.N., Pyatkov K.I., Kalinin A.E., Nesmeyanova M.A. Processing of Escherichia coli alkaline phosphatase. Sequence requirements and possible conformations of the -6 to -4 region of the signal peptide. J. Biol. Chem. 2002, 277:50396-50402.
23. Barkocy-Gallagher G.A., Bassford P.J. Synthesis of precursor maltose-binding protein with proline in the +1 position of the cleavage site interferes with the activity of Escherichia coli signal peptidase I in vivo. J. Biol. Chem. 1992, 267:1231-1238.
24. Wickner W., Moore K., Dibb N., Geissert D., Rice M. Inhibition of purified Escherichia coli leader peptidase by the leader (signal) peptide of bacteriophage M13 procoat. J. Bacteriol. 1987, 169:3821-3822.
25. Nilsson I., von Heijne G. A signal peptide with a proline next to the cleavage site inhibits leader peptidase when present in a sec-independent protein. FEBS Lett. 1992, 299:243-246.
26. Bechinger B., Gierasch L.M., Montal M., Zasloff M., Opella S.J. Orientations of helical peptides in membrane bilayers by solid state NMR spectroscopy. Solid State Nucl. Magn. Reson. 1996, 7:185-191.
27. Sankaram M.B., Marsh D., Gierasch L.M., Thompson T.E. Reorganization of lipid domain structure in membranes by a transmembrane peptide: an ESR spin label study on the effect of the Escherichia coli outer membrane protein A signal peptide on the fluid lipid domain connectivity in binary mixtures of dimyristoyl phosphatidylcholine and distearoyl phosphatidylcholine. Biophys. J. 1994, 66:1959-1968.
28. Wang Z., Jones J.D., Rizo J., Gierasch L.M. Membrane-bound conformation of a signal peptide: a transferred nuclear Overhauser effect analysis. Biochemistry 1993, 32:13991-13999.
29. Rizo J., Blanco F.J., Kobe B., Bruch M.D., Gierasch L.M. Conformational behavior of Escherichia coli OmpA signal peptides in membrane mimetic environments. Biochemistry 1993, 32:4881-4894.
30. McKnight C.J., Stradley S.J., Jones J.D., Gierasch L.M. Conformational and membrane-binding properties of a signal sequence are largely unaltered by its adjacent mature region. Proc. Natl. Acad. Sci. U. S. A. 1991, 88:5799-5803.
31. McKnight C.J., Rafalski M., Gierasch L.M. Fluorescence analysis of tryptophan-containing variants of the LamB signal sequence upon insertion into a lipid bilayer. Biochemistry 1991, 30:6241-6246.
32. Paetzel M., Dalbey R.E., Strynadka N.C. Crystal structure of a bacterial signal peptidase in complex with a beta-lactam inhibitor. Nature 1998, 396:186-190.
33. Luke I., Handford J.I., Palmer T., Sargent F. Proteolytic processing of Escherichia coli twin-arginine signal peptides by LepB. Arch. Microbiol. 2009, 191:919-925.
34. Palmer T., Berks B.C. The twin-arginine translocation (Tat) protein export pathway. Nat. Rev. Microbiol. 2012, 10:483-496.
35. Tullman-Ercek D., DeLisa M.P., Kawarasaki Y., Iranpour P., Ribnicky B., Palmer T., Georgiou G. Export pathway selectivity of Escherichia coli twin arginine translocation signal peptides. J. Biol. Chem. 2007, 282:8309-8316.
36. Chang C.N., Blobel G., Model P. Detection of prokaryotic signal peptidase in an Escherichia coli membrane fraction: endoproteolytic cleavage of nascent f1 pre-coat protein. Proc. Natl. Acad. Sci. U. S. A. 1978, 75:361-365.
37. Milstein C., Brownlee G.G., Harrison T.M., Mathews M.B. A possible precursor of immunoglobulin light chains. Nat. New Biol. 1972, 239:117-120.
38. Date T., Wickner W. Isolation of the Escherichia coli leader peptidase gene and effects of leader peptidase overproduction in vivo. Proc. Natl. Acad. Sci. U. S. A. 1981, 78:6106-6110.
39. Wolfe P.B., Wickner W., Goodman J.M. Sequence of the leader peptidase gene of Escherichia coli and the orientation of leader peptidase in the bacterial envelope. J. Biol. Chem. 1983, 258:12073-12080.
40. Wolfe P.B., Silver P., Wickner W. The isolation of homogeneous leader peptidase from a strain of Escherichia coli which overproduces the enzyme. J. Biol. Chem. 1982, 257:7898-7902.
41. Dalbey R.E., Wickner W. Leader peptidase catalyzes the release of exported proteins from the outer surface of the Escherichia coli plasma membrane. J. Biol. Chem. 1985, 260:15925-15931.
42. Tschantz W.R., Dalbey R.E. Bacterial leader peptidase 1. Methods Enzymol. 1994, 244:285-301.
43. Zwizinski C., Wickner W. Purification and characterization of leader (signal) peptidase from Escherichia coli. J. Biol. Chem. 1980, 255:7973-7977.
44. Sung M., Dalbey R.E. Identification of potential active-site residues in the Escherichia coli leader peptidase. J. Biol. Chem. 1992, 267:13154-13159.
45. Tschantz W.R., Sung M., Delgado-Partin V.M., Dalbey R.E. A serine and a lysine residue implicated in the catalytic mechanism of the Escherichia coli leader peptidase. J. Biol. Chem. 1993, 268:27349-27354.
46. Chatterjee S., Suciu D., Dalbey R.E., Kahn P.C., Inouye M. Determination of Km and kcat for signal peptidase I using a full length secretory precursor, pro-OmpA-nuclease A. J. Mol. Biol. 1995, 245:311-314.
47. Paetzel M., Strynadka N.C., Tschantz W.R., Casareno R., Bullinger P.R., Dalbey R.E. Use of site-directed chemical modification to study an essential lysine in Escherichia coli leader peptidase. J. Biol. Chem. 1997, 272:9994-10003.
48. van Klompenburg W., Whitley P., Diemel R., von Heijne G., de Kruijff B. A quantitative assay to determine the amount of signal peptidase I in E. coli and the orientation of membrane vesicles. Mol. Membr. Biol. 1995, 12:349-353.
49. Silver P., Wickner W. Genetic mapping of the Escherichia coli leader (signal) peptidase gene (lep): a new approach for determining the map position of a cloned gene. J. Bacteriol. 1983, 154:569-572.
50. Date T. Demonstration by a novel genetic technique that leader peptidase is an essential enzyme of Escherichia coli. J. Bacteriol. 1983, 154:76-83.
51. Inada T., Court D.L., Ito K., Nakamura Y. Conditionally lethal amber mutations in the leader peptidase gene of Escherichia coli. J. Bacteriol. 1989, 171:585-587.
52. Rawlings N.D., Barrett A.J., Bateman A. MEROPS: the peptidase database. Nucleic Acids Res. 2010, 38:D227-D233.
53. Kuo D.W., Chan H.K., Wilson C.J., Griffin P.R., Williams H., Knight W.B. Escherichia coli leader peptidase: production of an active form lacking a requirement for detergent and development of peptide substrates. Arch. Biochem. Biophys. 1993, 303:274-280.
54. Whitley P., von Heijne G. The DsbA-DsbB system affects the formation of disulfide bonds in periplasmic but not in intramembraneous protein domains. FEBS Lett. 1993, 332:49-51.
55. Moore K.E., Miura S. A small hydrophobic domain anchors leader peptidase to the cytoplasmic membrane of Escherichia coli. J. Biol. Chem. 1987, 262:8806-8813.
56. San Millan J.L., Boyd D., Dalbey R., Wickner W., Beckwith J. Use of phoA fusions to study the topology of the Escherichia coli inner membrane protein leader peptidase. J. Bacteriol. 1989, 171:5536-5541.
57. Whitley P., Nilsson L., von Heijne G. Three-dimensional model for the membrane domain of Escherichia coli leader peptidase based on disulfide mapping. Biochemistry 1993, 32:8534-8539.
58. Bilgin N., Lee J.I., Zhu H.Y., Dalbey R., von Heijne G. Mapping of catalytically important domains in Escherichia coli leader peptidase. EMBO J. 1990, 9:2717-2722.
59. Tschantz W.R., Paetzel M., Cao G., Suciu D., Inouye M., Dalbey R.E. Characterization of a soluble, catalytically active form of Escherichia coli leader peptidase: requirement of detergent or phospholipid for optimal activity. Biochemistry 1995, 34:3935-3941.
60. Talarico T.L., Dev I.K., Bassford P.J., Ray P.H. Inter-molecular degradation of signal peptidase I in vitro. Biochem. Biophys. Res. Commun. 1991, 181:650-656.
61. Wang Y., Bruckner R., Stein R.L. Regulation of signal peptidase by phospholipids in membrane: characterization of phospholipid bilayer incorporated Escherichia coli signal peptidase. Biochemistry 2004, 43:265-270.
62. Black M.T. Evidence that the catalytic activity of prokaryote leader peptidase depends upon the operation of a serine-lysine catalytic dyad. J. Bacteriol. 1993, 175:4957-4961.
63. Ray P., Dev I., MacGregor C., Bassford P. Signal peptidases. Curr. Top. Microbiol. Immunol. 1986, 125:75-102.
64. Gallagher J., Kaderbhai N.N., Kaderbhai M.A. Kinetic constants of signal peptidase I using cytochrome b5 as a precursor substrate. Biochim. Biophys. Acta 2001, 1550:1-5.
65. Suciu D., Chatterjee S., Inouye M. Catalytic efficiency of signal peptidase I of Escherichia coli is comparable to that of members of the serine protease family. Protein Eng. 1997, 10:1057-1060.
66. Zhong W., Benkovic S.J. Development of an internally quenched fluorescent substrate for Escherichia coli leader peptidase. Anal. Biochem. 1998, 255:66-73.
67. Stein R.L., Barbosa M.D., Bruckner R. Kinetic and mechanistic studies of signal peptidase I from Escherichia coli. Biochemistry 2000, 39:7973-7983.
68. Bruton G., Huxley A., O'Hanlon P., Orlek B., Eggleston D., Humphries J., Readshaw S., West A., Ashman S., Brown M., Moore K., Pope A., O'Dwyer K., Wang L. Lipopeptide substrates for SpsB, the Staphylococcus aureus type I signal peptidase: design, conformation and conversion to alpha-ketoamide inhibitors. Eur. J. Med. Chem. 2003, 38:351-356.
69. Ekici O.D., Zhu J., Wah Chung I.Y., Paetzel M., Dalbey R.E., Pei D. Profiling the substrate specificity of viral protease VP4 by a FRET-based peptide library approach. Biochemistry 2009, 48:5753-5759.
70. Rosse G., Kueng E., Page M.G., Schauer-Vukasinovic V., Giller T., Lahm H.W., Hunziker P., Schlatter D. Rapid identification of substrates for novel proteases using a combinatorial peptide library. J. Comb. Chem. 2000, 2:461-466.
71. Cregg K.M., Wilding I., Black M.T. Molecular cloning and expression of the spsB gene encoding an essential type I signal peptidase from Staphylococcus aureus. J. Bacteriol. 1996, 178:5712-5718.
72. Barbosa M.D., Lin S., Markwalder J.A., Mills J.A., DeVito J.A., Teleha C.A., Garlapati V., Liu C., Thompson A., Trainor G.L., Kurilla M.G., Pompliano D.L. Regulated expression of the Escherichia coli lepB gene as a tool for cellular testing of antimicrobial compounds that inhibit signal peptidase I in vitro. Antimicrob. Agents Chemother. 2002, 46:3549-3554.
73. Zwizinski C., Date T., Wickner W. Leader peptidase is found in both the inner and outer membranes of Escherichia coli. J. Biol. Chem. 1981, 256:3593-3597.
74. Black M.T., Munn J.G., Allsop A.E. On the catalytic mechanism of prokaryotic leader peptidase 1. Biochem. J. 1992, 282:539-543.
75. Kim Y.T., Muramatsu T., Takahashi K. Leader peptidase from Escherichia coli: overexpression, characterization, and inactivation by modification of tryptophan residues 300 and 310 with N-bromosuccinimide. J. Biochem. 1995, 117:535-544.
76. Kuo D., Weidner J., Griffin P., Shah S.K., Knight W.B. Determination of the kinetic parameters of Escherichia coli leader peptidase activity using a continuous assay: the pH dependence and time-dependent inhibition by beta-lactams are consistent with a novel serine protease mechanism. Biochemistry 1994, 33:8347-8354.
77. Black M.T., Bruton G. Inhibitors of bacterial signal peptidases. Curr. Pharm. Des. 1998, 4:133-154.
78. Allsop A., Brooks G., Edwards P.D., Kaura A.C., Southgate R. Inhibitors of bacterial signal peptidase: a series of 6-(substituted oxyethyl)penems. J. Antibiot. (Tokyo) 1996, 49:921-928.
79. Perry C.R., Ashby M.J., Elsmere S.A. Penems as research tools to investigate the activity of E.coli leader peptidase. Biochem. Soc. Trans. 1995, 23:548S.
80. Allsop A.E., Brooks G., Bruton G., Coulton S., Edwards P.D., Hatton I.K., Kaura A.C., McLean S.D., Pearson N.D., Smale T.C., Southgate R. Penem inhibitors of bacterial signal peptidase. Bioorg. Med. Chem. Lett. 1995, 5:443-448.
81. Harris D.A., Powers M.E., Romesberg F.E. Synthesis and biological evaluation of penem inhibitors of bacterial signal peptidase. Bioorg. Med. Chem. Lett. 2009, 19:3787-3790.
82. Schimana J., Gebhardt K., Holtzel A., Schmid D.G., Sussmuth R., Muller J., Pukall R., Fiedler H.P. Arylomycins A and B, new biaryl-bridged lipopeptide antibiotics produced by Streptomyces sp. Tu 6075. I. Taxonomy, fermentation, isolation and biological activities. J. Antibiot. (Tokyo) 2002, 55:565-570.
83. Holtzel A., Schmid D.G., Nicholson G.J., Stevanovic S., Schimana J., Gebhardt K., Fiedler H.P., Jung G. Arylomycins A and B, new biaryl-bridged lipopeptide antibiotics produced by Streptomyces sp. Tu 6075. II. Structure elucidation. J. Antibiot. (Tokyo) 2002, 55:571-577.
84. Liu J., Luo C., Smith P.A., Chin J.K., Page M.G., Paetzel M., Romesberg F.E. Synthesis and characterization of the arylomycin lipoglycopeptide antibiotics and the crystallographic analysis of their complex with signal peptidase. J. Am. Chem. Soc. 2011, 133:17869-17877.
85. Roberts T.C., Schallenberger M.A., Liu J., Smith P.A., Romesberg F.E. Initial efforts toward the optimization of arylomycins for antibiotic activity. J. Med. Chem. 2011, 54:4954-4963.
86. Roberts T.C., Smith P.A., Cirz R.T., Romesberg F.E. Structural and initial biological analysis of synthetic arylomycin A2. J. Am. Chem. Soc. 2007, 129:15830-15838.
87. Roberts T.C., Smith P.A., Romesberg F.E. Synthesis and biological characterization of arylomycin B antibiotics. J. Nat. Prod. 2011, 74:956-961.
88. Smith P.A., Powers M.E., Roberts T.C., Romesberg F.E. In vitro activities of arylomycin natural-product antibiotics against Staphylococcus epidermidis and other coagulase-negative staphylococci. Antimicrob. Agents Chemother. 2011, 55:1130-1134.
89. Smith P.A., Roberts T.C., Romesberg F.E. Broad-spectrum antibiotic activity of the arylomycin natural products is masked by natural target mutations. Chem. Biol. 2010, 17:1223-1231.
90. Smith P.A., Romesberg F.E. Mechanism of action of the arylomycin antibiotics and effects of signal peptidase I inhibition. Antimicrob. Agents Chemother. 2012, 56:5054-5060.
91. Liu W.T., Kersten R.D., Yang Y.L., Moore B.S., Dorrestein P.C. Imaging mass spectrometry and genome mining via short sequence tagging identified the anti-infective agent arylomycin in Streptomyces roseosporus. J. Am. Chem. Soc. 2011, 133:18010-18013.
92. Buzder-Lantos P., Bockstael K., Anne J., Herdewijn P. Substrate based peptide aldehyde inhibits bacterial type I signal peptidase. Bioorg. Med. Chem. Lett. 2009, 19:2880-2883.
93. Paetzel M., Chernaia M., Strynadka N., Tschantz W., Cao G., Dalbey R.E., James M.N. Crystallization of a soluble, catalytically active form of Escherichia coli leader peptidase. Proteins 1995, 23:122-125.
94. Dalbey R.E., Lively M.O., Bron S., van Dijl J.M. The chemistry and enzymology of the type I signal peptidases. Protein Sci. 1997, 6:1129-1138.
95. Paetzel M., Woodgate R. Chapter 773 - UmuD and UmuD' proteins. Handbook of Proteolytic Enzymes 2013, 3487-3492. Academic Press.
96. Paetzel M., Strynadka N.C. Common protein architecture and binding sites in proteases utilizing a Ser/Lys dyad mechanism. Protein Sci. 1999, 8:2533-2536.
97. Klenotic P.A., Carlos J.L., Samuelson J.C., Schuenemann T.A., Tschantz W.R., Paetzel M., Strynadka N.C., Dalbey R.E. The role of the conserved box E residues in the active site of the Escherichia coli type I signal peptidase. J. Biol. Chem. 2000, 275:6490-6498.
98. Carlos J.L., Klenotic P.A., Paetzel M., Strynadka N.C., Dalbey R.E. Mutational evidence of transition state stabilization by serine 88 in Escherichia coli type I signal peptidase. Biochemistry 2000, 39:7276-7283.
99. Tyndall J.D., Nall T., Fairlie D.P. Proteases universally recognize beta strands in their active sites. Chem. Rev. 2005, 105:973-999.
100. Karla A., Lively M.O., Paetzel M., Dalbey R. The identification of residues that control signal peptidase cleavage fidelity and substrate specificity. J. Biol. Chem. 2005, 280:6731-6741.
101. Ekici O.D., Karla A., Paetzel M., Lively M.O., Pei D., Dalbey R.E. Altered -3 substrate specificity of Escherichia coli signal peptidase 1 mutants as revealed by screening a combinatorial peptide library. J. Biol. Chem. 2007, 282:417-425.
102. Paetzel M., Dalbey R.E., Strynadka N.C. Crystal structure of a bacterial signal peptidase apoenzyme: implications for signal peptide binding and the Ser-Lys dyad mechanism. J. Biol. Chem. 2002, 277:9512-9519.
103. Paetzel M., Goodall J.J., Kania M., Dalbey R.E., Page M.G. Crystallographic and biophysical analysis of a bacterial signal peptidase in complex with a lipopeptide-based inhibitor. J. Biol. Chem. 2004, 279:30781-30790.
104. Luo C., Roussel P., Dreier J., Page M.G., Paetzel M. Crystallographic analysis of bacterial signal peptidase in ternary complex with arylomycin A2 and a beta-sultam inhibitor. Biochemistry 2009, 48:8976-8984.
105. Luo Y., Pfuetzner R.A., Mosimann S., Paetzel M., Frey E.A., Cherney M., Kim B., Little J.W., Strynadka N.C. Crystal structure of LexA: a conformational switch for regulation of self-cleavage. Cell 2001, 106:585-594.
106. Musial-Siwek M., Kendall D.A., Yeagle P.L. Solution NMR of signal peptidase, a membrane protein. Biochim. Biophys. Acta 2008, 1778:937-944.
107. Musial-Siwek M., Yeagle P.L., Kendall D.A. A small subset of signal peptidase residues are perturbed by signal peptide binding. Chem. Biol. Drug Des. 2008, 72:140-146.
108. De Bona P., Deshmukh L., Gorbatyuk V., Vinogradova O., Kendall D.A. Structural studies of a signal peptide in complex with signal peptidase I cytoplasmic domain: the stabilizing effect of membrane-mimetics on the acquired fold. Proteins 2012, 80:807-817.
109. Carlos J.L., Paetzel M., Brubaker G., Karla A., Ashwell C.M., Lively M.O., Cao G., Bullinger P., Dalbey R.E. The role of the membrane-spanning domain of type I signal peptidases in substrate cleavage site selection. J. Biol. Chem. 2000, 275:38813-38822.
110. Dierstein R., Wickner W. Requirements for substrate recognition by bacterial leader peptidase. EMBO J. 1986, 5:427-431.
111. Watts C., Silver P., Wickner W. Membrane assembly from purified components. II. Assembly of M13 procoat into liposomes reconstituted with purified leader peptidase. Cell 1981, 25:347-353.
112. Ohno-Iwashita Y., Wolfe P., Ito K., Wickner W. Processing of preproteins by liposomes bearing leader peptidase. Biochemistry 1984, 23:6178-6184.
113. van Klompenburg W., Paetzel M., de Jong J.M., Dalbey R.E., Demel R.A., von Heijne G., de Kruijff B. Phosphatidylethanolamine mediates insertion of the catalytic domain of leader peptidase in membranes. FEBS Lett. 1998, 431:75-79.
114. Kim Y.T., Muramatsu T., Takahashi K. Identification of Trp300 as an important residue for Escherichia coli leader peptidase activity. Eur. J. Biochem. 1995, 234:358-362.
115. Carlos J.L., Paetzel M., Klenotic P.A., Strynadka N.C.J., Dalbey R.E. Bacterial type I signal peptidases. The Enzymes 2002, volume 22:27-55. Academic Press. E.D. Rose, S.S. David (Eds.).
116. Paetzel M., Dalbey R.E., Strynadka N.C. The structure and mechanism of bacterial type I signal peptidases. A novel antibiotic target. Pharmacol. Ther. 2000, 87:27-49.
117. Paetzel M., Karla A., Strynadka N.C., Dalbey R.E. Signal peptidases. Chem. Rev. 2002, 102:4549-4580.
118. Freeman M. Rhomboid proteases and their biological functions. Annu. Rev. Genet. 2008, 42:191-210.
119. Erez E., Fass D., Bibi E. How intramembrane proteases bury hydrolytic reactions in the membrane. Nature 2009, 459:371-378.
120. Kim A.C., Oliver D.C., Paetzel M. Crystal structure of a bacterial signal peptide peptidase. J. Mol. Biol. 2008, 376:352-366.
121. Wang P., Shim E., Cravatt B., Jacobsen R., Schoeniger J., Kim A.C., Paetzel M., Dalbey R.E. Escherichia coli signal peptide peptidase A is a serine-lysine protease with a lysine recruited to the nonconserved amino-terminal domain in the S49 protease family. Biochemistry 2008, 47:6361-6369.
122. Barbrook A.C., Packer J.C., Howe C.J. Inhibition by penem of processing peptidases from cyanobacteria and chloroplast thylakoids. FEBS Lett. 1996, 398:198-200.
123. Bockstael K., Geukens N., Rao C.V., Herdewijn P., Anne J., Van Aerschot A. An easy and fast method for the evaluation of Staphylococcus epidermidis type I signal peptidase inhibitors. J. Microbiol. Methods 2009, 78:231-237.