Review Article

Bacterial Metalo-Aminopeptidases as Targets in Human Infectious Diseases

Author(s): Jorge González-Bacerio*, Ana C. Varela, Mirtha E. Aguado, Maikel Izquierdo, Yanira Méndez, Maday A. del Rivero and Daniel G. Rivera

Volume 23, Issue 12, 2022

Published on: 22 July, 2022

Page: [1155 - 1190] Pages: 36

DOI: 10.2174/1389450123666220316085859

Price: $65

Abstract

Background: Human infectious diseases caused by bacteria are a worldwide health problem due to the increased resistance of these microorganisms to conventional antibiotics. For this reason, the identification of novel molecular targets and the discovery of new antibacterial compounds are urgently required. Metalo-aminopeptidases are promising targets in bacterial infections. They participate in crucial processes for bacterial growth and pathogenesis, such as protein and peptide degradation to supply amino acids, protein processing, access to host tissues, cysteine supply for redox control, transcriptional regulation, site-specific DNA recombination, and hydrogen sulfide production. Although several of these enzymes are not essential, they are required for virulence and maximal growth in conditions of nutrient limitation and high temperatures.

Objective: In this review, we describe the structural, functional, and kinetic properties of some examples of bacterial metalo-aminopeptidases, in the context of their use as antibacterial targets. In addition, we present some inhibitors reported for these enzymes.

Conclusion: It is necessary to conduct a meticulous work to validate these peptidases as good/bad targets and to identify inhibitors with potential therapeutic use.

Keywords: Antibacterial agents, divalent metallic cations, enzyme-inhibitor complexes, metalo-aminopeptidases, pathogenic bacteria, protease inhibitors.

Graphical Abstract
[1]
Taylor A. Aminopeptidases: Structure and function. FASEB J 1993; 7(2): 290-8.
[http://dx.doi.org/10.1096/fasebj.7.2.8440407] [PMID: 8440407]
[2]
Booth M, Jennings V, Fhaolain IN, O’Cuinn G. Prolidase activity of Lactococcus lactis subsp. cremoris AM2: Partial purification and characterization. J Dairy Res 1990; 57(2): 245-54.
[http://dx.doi.org/10.1017/S0022029900026868]
[3]
Smid EJ, Poolman B, Konings WN. Casein utilization by lactococci. Appl Environ Microbiol 1991; 57(9): 2447-52.
[http://dx.doi.org/10.1128/aem.57.9.2447-2452.1991] [PMID: 1768119]
[4]
Goldberg AL, Dice JF. Intracellular protein degradation in mammalian and bacterial cells. Annu Rev Biochem 1974; 43(0): 835-69.
[http://dx.doi.org/10.1146/annurev.bi.43.070174.004155] [PMID: 4604628]
[5]
Goldberg AL, St John AC. Intracellular protein degradation in mammalian and bacterial cells: Part 2. Annu Rev Biochem 1976; 45: 747-803.
[http://dx.doi.org/10.1146/annurev.bi.45.070176.003531] [PMID: 786161]
[6]
Lazdunski AM. Peptidases and proteases of Escherichia coli and Salmonella typhimurium. FEMS Microbiol Rev 1989; 5(3): 265-76.
[http://dx.doi.org/10.1016/0168-6445(89)90035-1] [PMID: 2698230]
[7]
Miller CG. Peptidases and proteases of Escherichia coli and Salmonella typhimurium. Annu Rev Microbiol 1975; 29(1): 485-504.
[http://dx.doi.org/10.1146/annurev.mi.29.100175.002413] [PMID: 1101808]
[8]
Niven GW. Purification and characterization of aminopeptidase A from Lactococcus lactis subsp. lactis NCDO712. J Gen Microbiol 1991; 137(5): 1207-12.
[http://dx.doi.org/10.1099/00221287-137-5-1207]
[9]
Rawlings ND, Waller M, Barrett AJ, Bateman A. MEROPS: The database of proteolytic enzymes, their substrates and inhibitors. Nucleic Acids Res 2014; 42(Database issue): D503-9.
[http://dx.doi.org/10.1093/nar/gkt953] [PMID: 24157837]
[10]
Klinke T, Rump A, Pönisch R, et al. Identification and characterization of CaApe2--a neutral arginine/alanine/leucine-specific metallo-aminopeptidase from Candida albicans. FEMS Yeast Res 2008; 8(6): 858-69.
[http://dx.doi.org/10.1111/j.1567-1364.2008.00411.x] [PMID: 18637841]
[11]
Albiston AL, Ye S, Chai SY. Membrane bound members of the M1 family: More than aminopeptidases. Protein Pept Lett 2004; 11(5): 491-500.
[http://dx.doi.org/10.2174/0929866043406643] [PMID: 15544570]
[12]
Rozenfeld R, Muller L, El Messari S, Llorens-Cortes C. The C-terminal domain of aminopeptidase A is an intramolecular chaperone required for the correct folding, cell surface expression, and activity of this monozinc aminopeptidase. J Biol Chem 2004; 279(41): 43285-95.
[http://dx.doi.org/10.1074/jbc.M404369200] [PMID: 15263000]
[13]
Chávez-Gutiérrez L, Bourdais J, Aranda G, et al. A truncated isoform of pyroglutamyl aminopeptidase II produced by exon extension has dominant-negative activity. J Neurochem 2005; 92(4): 807-17.
[http://dx.doi.org/10.1111/j.1471-4159.2004.02916.x] [PMID: 15686482]
[14]
Haeggström JZ, Kull F, Rudberg PC, Tholander F, Thunnissen MM. Leukotriene A4 hydrolase. Prostagl Other Lipid Mediat 2002; 68-69: 495-510.
[http://dx.doi.org/10.1016/S0090-6980(02)00051-5] [PMID: 12432939]
[15]
Piesse C, Tymms M, Garrafa E, et al. Human aminopeptidase B (rnpep) on chromosome 1q32.2: Complementary DNA, genomic structure and expression. Gene 2002; 292(1-2): 129-40.
[http://dx.doi.org/10.1016/S0378-1119(02)00650-9] [PMID: 12119107]
[16]
Díaz-Perales A, Quesada V, Sánchez LM, et al. Identification of human aminopeptidase O, a novel metalloprotease with structural similarity to aminopeptidase B and leukotriene A4 hydrolase. J Biol Chem 2005; 280(14): 14310-7.
[http://dx.doi.org/10.1074/jbc.M413222200] [PMID: 15687497]
[17]
Rawlings ND, Barrett AJ. Evolutionary families of metallopeptidases. Methods Enzymol 1995; 248: 183-228.
[http://dx.doi.org/10.1016/0076-6879(95)48015-3] [PMID: 7674922]
[18]
Mucha A, Drag M, Dalton JP, Kafarski P. Metallo-aminopeptidase inhibitors. Biochimie 2010; 92(11): 1509-29.
[http://dx.doi.org/10.1016/j.biochi.2010.04.026] [PMID: 20457213]
[19]
Dalal S, Ragheb DRT, Schubot FD, Klemba M. A naturally variable residue in the S1 subsite of M1 family aminopeptidases modulates catalytic properties and promotes functional specialization. J Biol Chem 2013; 288(36): 26004-12.
[http://dx.doi.org/10.1074/jbc.M113.465625] [PMID: 23897806]
[20]
Schechter I, Berger A. On the size of the active site in proteases. I. Papain. Biochem Biophys Res Commun 1967; 27(2): 157-62.
[http://dx.doi.org/10.1016/S0006-291X(67)80055-X] [PMID: 6035483]
[21]
Allary M, Schrével J, Florent I. Properties, stage-dependent expression and localization of Plasmodium falciparum M1 family zinc-aminopeptidase. Parasitology 2002; 125(Pt 1): 1-10.
[http://dx.doi.org/10.1017/S0031182002001828] [PMID: 12166515]
[22]
Cadavid-Restrepo G, Gastardelo TS, Faudry E, et al. The major leucyl aminopeptidase of Trypanosoma cruzi (LAPTc) assembles into a homohexamer and belongs to the M17 family of metallopeptidases. BMC Biochem 2011; 12(1): 46.
[http://dx.doi.org/10.1186/1471-2091-12-46] [PMID: 21861921]
[23]
Florent I, Derhy Z, Allary M, Monsigny M, Mayer R, Schrével J. A Plasmodium falciparum aminopeptidase gene belonging to the M1 family of zinc-metallopeptidases is expressed in erythrocytic stages. Mol Biochem Parasitol 1998; 97(1-2): 149-60.
[http://dx.doi.org/10.1016/S0166-6851(98)00143-1] [PMID: 9879894]
[24]
Chandu D, Nandi D. PepN is the major aminopeptidase in Escherichia coli: Insights on substrate specificity and role during sodium-salicylate-induced stress. Microbiology 2003; 149(Pt 12): 3437-47.
[http://dx.doi.org/10.1099/mic.0.26518-0] [PMID: 14663077]
[25]
Addlagatta A, Gay L, Matthews BW. Structural basis for the unusual specificity of Escherichia coli aminopeptidase N. Biochemistry 2008; 47(19): 5303-11.
[http://dx.doi.org/10.1021/bi7022333] [PMID: 18416562]
[26]
Luan Y, Xu W. The structure and main functions of aminopeptidase N. Curr Med Chem 2007; 14(6): 639-47.
[http://dx.doi.org/10.2174/092986707780059571] [PMID: 17346152]
[27]
Maroux S, Louvard D, Baratti J. The aminopeptidase from hog intestinal brush border. Biochim Biophys Acta 1973; 321(1): 282-95.
[http://dx.doi.org/10.1016/0005-2744(73)90083-1] [PMID: 4750768]
[28]
Noble F, Roques BP. Protection of endogenous enkephalin catabolism as natural approach to novel analgesic and antidepressant drugs. Expert Opin Ther Targets 2007; 11(2): 145-59.
[http://dx.doi.org/10.1517/14728222.11.2.145] [PMID: 17227231]
[29]
Yamashita M, Kajiyama H, Terauchi M, et al. Involvement of aminopeptidase N in enhanced chemosensitivity to paclitaxel in ovarian carcinoma in vitro and in vivo. Int J Cancer 2007; 120(10): 2243-50.
[http://dx.doi.org/10.1002/ijc.22528] [PMID: 17266036]
[30]
Saiki I, Fujii H, Yoneda J, et al. Role of aminopeptidase N (CD13) in tumor-cell invasion and extracellular matrix degradation. Int J Cancer 1993; 54(1): 137-43.
[http://dx.doi.org/10.1002/ijc.2910540122] [PMID: 8097496]
[31]
Rangel R, Sun Y, Guzman-Rojas L, et al. Impaired angiogenesis in aminopeptidase N-null mice. Proc Natl Acad Sci USA 2007; 104(11): 4588-93.
[http://dx.doi.org/10.1073/pnas.0611653104] [PMID: 17360568]
[32]
Bauvois B, Dauzonne D. Aminopeptidase-N/CD13 (EC 3.4.11.2) inhibitors: Chemistry, biological evaluations, and therapeutic prospects. Med Res Rev 2006; 26(1): 88-130.
[http://dx.doi.org/10.1002/med.20044] [PMID: 16216010]
[33]
Harbut MB, Velmourougane G, Dalal S, et al. Bestatin-based chemical biology strategy reveals distinct roles for malaria M1- and M17-family aminopeptidases. Proc Natl Acad Sci USA 2011; 108(34): E526-34.
[http://dx.doi.org/10.1073/pnas.1105601108] [PMID: 21844374]
[34]
Shimizu T, Tani K, Hase K, et al. CD13/aminopeptidase N-induced lymphocyte involvement in inflamed joints of patients with rheumatoid arthritis. Arthritis Rheum 2002; 46(9): 2330-8.
[http://dx.doi.org/10.1002/art.10517] [PMID: 12355480]
[35]
Bedir A, Ozener IC, Emerk K. Urinary leucine aminopeptidase is a more sensitive indicator of early renal damage in non-insulin-dependent diabetics than microalbuminuria. Nephron J 1996; 74(1): 110-3.
[http://dx.doi.org/10.1159/000189288] [PMID: 8883027]
[36]
Sloane PD, Zimmerman S, Suchindran C, et al. The public health impact of Alzheimer’s disease, 2000-2050: Potential implication of treatment advances. Annu Rev Public Health 2002; 23(1): 213-31.
[http://dx.doi.org/10.1146/annurev.publhealth.23.100901.140525] [PMID: 11910061]
[37]
Reinhold D, Biton A, Pieper S, et al. Dipeptidyl peptidase IV (DP IV, CD26) and aminopeptidase N (APN, CD13) as regulators of T cell function and targets of immunotherapy in CNS inflammation. Int Immunopharmacol 2006; 6(13-14): 1935-42.
[http://dx.doi.org/10.1016/j.intimp.2006.07.023] [PMID: 17161346]
[38]
Thielitz A, Ansorge S, Bank U, et al. The ectopeptidases dipeptidyl peptidase IV (DP IV) and aminopeptidase N (APN) and their related enzymes as possible targets in the treatment of skin diseases. Front Biosci 2008; 13(13): 2364-75.
[http://dx.doi.org/10.2741/2850] [PMID: 17981718]
[39]
Ito K, Nakajima Y, Onohara Y, et al. Crystal structure of aminopeptidase N (proteobacteria alanyl aminopeptidase) from Escherichia coli and conformational change of methionine 260 involved in substrate recognition. J Biol Chem 2006; 281(44): 33664-76.
[http://dx.doi.org/10.1074/jbc.M605203200] [PMID: 16885166]
[40]
Burley SK, David PR, Taylor A, Lipscomb WN. Molecular structure of leucine aminopeptidase at 2.7-A resolution. Proc Natl Acad Sci USA 1990; 87(17): 6878-82.
[http://dx.doi.org/10.1073/pnas.87.17.6878] [PMID: 2395881]
[41]
Matsui M, Fowler JH, Walling LL. Leucine aminopeptidases: Diversity in structure and function. Biol Chem 2006; 387(12): 1535-44.
[http://dx.doi.org/10.1515/BC.2006.191] [PMID: 17132098]
[42]
Scranton MA, Yee A, Park SY, Walling LL. Plant leucine aminopeptidases moonlight as molecular chaperones to alleviate stress-induced damage. J Biol Chem 2012; 287(22): 18408-17.
[http://dx.doi.org/10.1074/jbc.M111.309500] [PMID: 22493451]
[43]
Behari J, Stagon L, Calderwood SB. pepA, a gene mediating pH regulation of virulence genes in Vibrio cholerae. J Bacteriol 2001; 183(1): 178-88.
[http://dx.doi.org/10.1128/JB.183.1.178-188.2001] [PMID: 11114915]
[44]
Alén C, Sherratt DJ, Colloms SD. Direct interaction of aminopeptidase A with recombination site DNA in Xer site-specific recombination. EMBO J 1997; 16(17): 5188-97.
[http://dx.doi.org/10.1093/emboj/16.17.5188] [PMID: 9311979]
[45]
Lowther WT, Matthews BW. Metalloaminopeptidases: Common functional themes in disparate structural surroundings. Chem Rev 2002; 102(12): 4581-608.
[http://dx.doi.org/10.1021/cr0101757] [PMID: 12475202]
[46]
Carroll RK, Robison TM, Rivera FE, et al. Identification of an intracellular M17 family leucine aminopeptidase that is required for virulence in Staphylococcus aureus. Microbes Infect 2012; 14(11): 989-99.
[http://dx.doi.org/10.1016/j.micinf.2012.04.013] [PMID: 22613209]
[47]
Drinkwater N, Malcolm TR, McGowan S. M17 aminopeptidases diversify function by moderating their macromolecular assemblies and active site environment. Biochimie 2019; 166: 38-51.
[http://dx.doi.org/10.1016/j.biochi.2019.01.007] [PMID: 30654132]
[48]
McGowan S, Oellig CA, Birru WA, et al. Structure of the Plasmodium falciparum M17 aminopeptidase and significance for the design of drugs targeting the neutral exopeptidases. Proc Natl Acad Sci USA 2010; 107(6): 2449-54.
[http://dx.doi.org/10.1073/pnas.0911813107] [PMID: 20133789]
[49]
Duprez K, Scranton MA, Walling LL, Fan L. Structure of tomato wound-induced leucine aminopeptidase sheds light on substrate specificity. Acta Crystallogr D Biol Crystallogr 2014; 70(Pt 6): 1649-58.
[http://dx.doi.org/10.1107/S1399004714006245] [PMID: 24914976]
[50]
Modak JK, Rut W, Wijeyewickrema LC, Pike RN, Drag M, Roujeinikova A. Structural basis for substrate specificity of Helicobacter pylori M17 aminopeptidase. Biochimie 2016; 121: 60-71.
[http://dx.doi.org/10.1016/j.biochi.2015.11.021] [PMID: 26616008]
[51]
Gu YQ, Holzer FM, Walling LL. Overexpression, purification and biochemical characterization of the wound-induced leucine aminopeptidase of tomato. Eur J Biochem 1999; 263(3): 726-35.
[http://dx.doi.org/10.1046/j.1432-1327.1999.00548.x] [PMID: 10469136]
[52]
Allen MP, Yamada AH, Carpenter FH. Kinetic parameters of metal-substituted leucine aminopeptidase from bovine lens. Biochemistry 1983; 22(16): 3778-83.
[http://dx.doi.org/10.1021/bi00285a010] [PMID: 6615800]
[53]
Carpenter FH, Vahl JM. Leucine aminopeptidase (Bovine lens). Mechanism of activation by Mg 2+ and Mn 2+ of the zinc metalloenzyme, amino acid composition, and sulfhydryl content. J Biol Chem 1973; 248(1): 294-304.
[http://dx.doi.org/10.1016/S0021-9258(19)44474-8] [PMID: 4692835]
[54]
Thompson GA, Carpenter FH. Leucine aminopeptidase (bovine lens). The relative binding of cobalt and zinc to leucine aminopeptidase and the effect of cobalt substitution on specific activity. J Biol Chem 1976; 251(6): 1618-24.
[http://dx.doi.org/10.1016/S0021-9258(17)33693-1] [PMID: 1254587]
[55]
Van Wart HE, Lin SH. Metal binding stoichiometry and mechanism of metal ion modulation of the activity of porcine kidney leucine aminopeptidase. Biochemistry 1981; 20(20): 5682-9.
[http://dx.doi.org/10.1021/bi00523a007] [PMID: 7295698]
[56]
Kim H, Lipscomb WN. Differentiation and identification of the two catalytic metal binding sites in bovine lens leucine aminopeptidase by x-ray crystallography. Proc Natl Acad Sci USA 1993; 90(11): 5006-10.
[http://dx.doi.org/10.1073/pnas.90.11.5006] [PMID: 8506345]
[57]
Cappiello M, Alterio V, Amodeo P, et al. Metal ion substitution in the catalytic site greatly affects the binding of sulfhydryl-containing compounds to leucyl aminopeptidase. Biochemistry 2006; 45(10): 3226-34.
[http://dx.doi.org/10.1021/bi052069v] [PMID: 16519517]
[58]
Maric S, Donnelly SM, Robinson MW, et al. The M17 leucine aminopeptidase of the malaria parasite Plasmodium falciparum: Importance of active site metal ions in the binding of substrates and inhibitors. Biochemistry 2009; 48(23): 5435-9.
[http://dx.doi.org/10.1021/bi9003638] [PMID: 19408962]
[59]
Kim H, Lipscomb WN. X-ray crystallographic determination of the structure of bovine lens leucine aminopeptidase complexed with amastatin: Formulation of a catalytic mechanism featuring a gem-diolate transition state. Biochemistry 1993; 32(33): 8465-78.
[http://dx.doi.org/10.1021/bi00084a011] [PMID: 8357796]
[60]
Sträter N, Lipscomb WN. Two-metal ion mechanism of bovine lens leucine aminopeptidase: Active site solvent structure and binding mode of L-leucinal, a gem-diolate transition state analogue, by X-ray crystallography. Biochemistry 1995; 34(45): 14792-800.
[http://dx.doi.org/10.1021/bi00045a021] [PMID: 7578088]
[61]
Sträter N, Sun L, Kantrowitz ER, Lipscomb WN. A bicarbonate ion as a general base in the mechanism of peptide hydrolysis by dizinc leucine aminopeptidase. Proc Natl Acad Sci USA 1999; 96(20): 11151-5.
[http://dx.doi.org/10.1073/pnas.96.20.11151] [PMID: 10500145]
[62]
Zhu X, Barman A, Ozbil M, Zhang T, Li S, Prabhakar R. Mechanism of peptide hydrolysis by co-catalytic metal centers containing leucine aminopeptidase enzyme: A DFT approach. Eur J Biochem 2012; 17(2): 209-22.
[http://dx.doi.org/10.1007/s00775-011-0843-2] [PMID: 21918843]
[63]
Vogt VM. Purification and properties of an aminopeptidase from Escherichia coli. J Biol Chem 1970; 245(18): 4760-9.
[http://dx.doi.org/10.1016/S0021-9258(18)62858-3] [PMID: 4917241]
[64]
Gu Y-Q, Walling LL. Specificity of the wound-induced leucine aminopeptidase (LAP-A) of tomato activity on dipeptide and tripeptide substrates. Eur J Biochem 2000; 267(4): 1178-87.
[http://dx.doi.org/10.1046/j.1432-1327.2000.01116.x] [PMID: 10672029]
[65]
Gu YQ, Walling LL. Identification of residues critical for activity of the wound-induced leucine aminopeptidase (LAP-A) of tomato. Eur J Biochem 2002; 269(6): 1630-40.
[http://dx.doi.org/10.1046/j.1432-1327.2002.02795.x] [PMID: 11895433]
[66]
Liu S, Widom J, Kemp CW, Crews CM, Clardy J. Structure of human methionine aminopeptidase-2 complexed with fumagillin. Science 1998; 282(5392): 1324-7.
[http://dx.doi.org/10.1126/science.282.5392.1324] [PMID: 9812898]
[67]
Ma Z-Q, Xie S-X, Huang Q-Q, Nan F-J, Hurley TD, Ye Q-Z. Structural analysis of inhibition of E. coli methionine aminopeptidase: Implication of loop adaptability in selective inhibition of bacterial enzymes. BMC Struct Biol 2007; 7(1): 84.
[http://dx.doi.org/10.1186/1472-6807-7-84] [PMID: 18093325]
[68]
Lowther WT, Matthews BW. Structure and function of the methionine aminopeptidases. Biochim Biophys Acta 2000; 1477(1-2): 157-67.
[http://dx.doi.org/10.1016/S0167-4838(99)00271-X] [PMID: 10708856]
[69]
Boutin JA. Myristoylation. Cell Signal 1997; 9(1): 15-35.
[http://dx.doi.org/10.1016/S0898-6568(96)00100-3] [PMID: 9067626]
[70]
Giglione C, Boularot A, Meinnel T. Protein N-terminal methionine excision. Cell Mol Life Sci 2004; 61(12): 1455-74.
[http://dx.doi.org/10.1007/s00018-004-3466-8] [PMID: 15197470]
[71]
Chen X, Xie S, Bhat S, Kumar N, Shapiro TA, Liu JO. Fumagillin and fumarranol interact with P. falciparum methionine aminopeptidase 2 and inhibit malaria parasite growth in vitro and in vivo. Chem Biol 2009; 16(2): 193-202.
[http://dx.doi.org/10.1016/j.chembiol.2009.01.006] [PMID: 19246010]
[72]
Hirel PH, Schmitter MJ, Dessen P, Fayat G, Blanquet S. Extent of N-terminal methionine excision from Escherichia coli proteins is governed by the side-chain length of the penultimate amino acid. Proc Natl Acad Sci USA 1989; 86(21): 8247-51.
[http://dx.doi.org/10.1073/pnas.86.21.8247] [PMID: 2682640]
[73]
Addlagatta A, Hu X, Liu JO, Matthews BW. Structural basis for the functional differences between type I and type II human methionine aminopeptidases. Biochemistry 2005; 44(45): 14741-9.
[http://dx.doi.org/10.1021/bi051691k] [PMID: 16274222]
[74]
Zhang P, Nicholson DE, Bujnicki JM, et al. Angiogenesis inhibitors specific for methionine aminopeptidase 2 as drugs for malaria and leishmaniasis. J Biomed Sci 2002; 9(1): 34-40.
[http://dx.doi.org/10.1007/BF02256576] [PMID: 11810023]
[75]
Bradshaw RA, Brickey WW, Walker KW. N-terminal processing: The methionine aminopeptidase and N alpha-acetyl transferase families. Trends Biochem Sci 1998; 23(7): 263-7.
[http://dx.doi.org/10.1016/S0968-0004(98)01227-4] [PMID: 9697417]
[76]
Alvarado JJ, Nemkal A, Sauder JM, et al. Structure of a microsporidian methionine aminopeptidase type 2 complexed with fumagillin and TNP-470. Mol Biochem Parasitol 2009; 168(2): 158-67.
[http://dx.doi.org/10.1016/j.molbiopara.2009.07.008] [PMID: 19660503]
[77]
Hu XV, Chen X, Han KC, Mildvan AS, Liu JO. Kinetic and mutational studies of the number of interacting divalent cations required by bacterial and human methionine aminopeptidases. Biochemistry 2007; 46(44): 12833-43.
[http://dx.doi.org/10.1021/bi701127x] [PMID: 17929833]
[78]
Mauriz JL, Martín-Renedo J, García-Palomo A, Tuñón MJ, González-Gallego J. Methionine aminopeptidases as potential targets for treatment of gastrointestinal cancers and other tumours. Curr Drug Targets 2010; 11(11): 1439-57.
[http://dx.doi.org/10.2174/1389450111009011439] [PMID: 20583970]
[79]
Datta B, Ray MK, Chakrabarti D, Wylie DE, Gupta NK. Glycosylation of eukaryotic peptide chain initiation factor 2 (eIF-2)-associated 67-kDa polypeptide (p67) and its possible role in the inhibition of eIF-2 kinase-catalyzed phosphorylation of the eIF-2 alpha-subunit. J Biol Chem 1989; 264(34): 20620-4.
[http://dx.doi.org/10.1016/S0021-9258(19)47108-1] [PMID: 2511207]
[80]
Calcagno S, Klein CD. N-Terminal methionine processing by the zinc-activated Plasmodium falciparum methionine aminopeptidase 1b. Appl Microbiol Biotechnol 2016; 100(16): 7091-102.
[http://dx.doi.org/10.1007/s00253-016-7470-3] [PMID: 27023914]
[81]
Kanudia P, Mittal M, Kumaran S, Chakraborti PK. Amino-terminal extension present in the methionine aminopeptidase type 1c of Mycobacterium tuberculosis is indispensible for its activity. BMC Biochem 2011; 12(1): 35.
[http://dx.doi.org/10.1186/1471-2091-12-35] [PMID: 21729287]
[82]
Chatterjee M, Chatterjee N, Datta R, Datta B, Gupta NK. Expression and activity of p67 are induced during heat shock. Biochem Biophys Res Commun 1998; 249(1): 113-7.
[http://dx.doi.org/10.1006/bbrc.1998.9056] [PMID: 9705841]
[83]
D’souza VM, Bennett B, Copik AJ, Holz RC. Divalent metal binding properties of the methionyl aminopeptidase from Escherichia coli. Biochemistry 2000; 39(13): 3817-26.
[http://dx.doi.org/10.1021/bi9925827] [PMID: 10736182]
[84]
Yang G, Kirkpatrick RB, Ho T, et al. Steady-state kinetic characterization of substrates and metal-ion specificities of the full-length and N-terminally truncated recombinant human methionine aminopeptidases (type 2). Biochemistry 2001; 40(35): 10645-54.
[http://dx.doi.org/10.1021/bi010806r] [PMID: 11524009]
[85]
Meng L, Ruebush S, D’souza VM, Copik AJ, Tsunasawa S, Holz RC. Overexpression and divalent metal binding properties of the methionyl aminopeptidase from Pyrococcus furiosus. Biochemistry 2002; 41(23): 7199-208.
[http://dx.doi.org/10.1021/bi020138p] [PMID: 12044150]
[86]
Marschner A, Klein CD. Metal promiscuity and metal-dependent substrate preferences of Trypanosoma brucei methionine aminopeptidase 1. Biochimie 2015; 115: 35-43.
[http://dx.doi.org/10.1016/j.biochi.2015.04.012] [PMID: 25921435]
[87]
Lu JP. Catalysis and inhibition of Mycobacterium tuberculosis methionine aminopeptidase. J Med Chem 2010; 53(3): 1329.
[88]
Kishor C, Arya T, Reddi R, et al. Identification, biochemical and structural evaluation of species-specific inhibitors against type I methionine aminopeptidases. J Med Chem 2013; 56(13): 5295-305.
[http://dx.doi.org/10.1021/jm400395p] [PMID: 23767698]
[89]
Chang SY, McGary EC, Chang S. Methionine aminopeptidase gene of Escherichia coli is essential for cell growth. J Bacteriol 1989; 171(7): 4071-2.
[http://dx.doi.org/10.1128/jb.171.7.4071-4072.1989] [PMID: 2544569]
[90]
Li X, Chang Y-H. Amino-terminal protein processing in Saccharomyces cerevisiae is an essential function that requires two distinct methionine aminopeptidases. Proc Natl Acad Sci USA 1995; 92(26): 12357-61.
[http://dx.doi.org/10.1073/pnas.92.26.12357] [PMID: 8618900]
[91]
Altmeyer M, Amtmann E, Heyl C, Marschner A, Scheidig AJ, Klein CD. Beta-aminoketones as prodrugs for selective irreversible inhibitors of type-1 methionine aminopeptidases. Bioorg Med Chem Lett 2014; 24(22): 5310-4.
[http://dx.doi.org/10.1016/j.bmcl.2014.09.047] [PMID: 25293447]
[92]
Paterson DL. Infections due to other members of the Enterobacteriaceae, including management of multidrug-resistant strains Goldman’s Cecil medicine. 24th ed. Philadelphia: Elsevier Saunders 2011; pp. 1874-7.
[93]
Madigan M, Martinko JM, Stahl DA, Clark DP, Eds. Brock biology of microorganisms. 13th ed. San Francisco: Pearson Education Inc. 2012.
[94]
Riveros M, Ochoa TJ. Enteropatógenos de importancia en salud pública. Rev Peru Med Exp Salud Publica 2015; 32(1): 157-64.
[http://dx.doi.org/10.17843/rpmesp.2015.321.1588] [PMID: 26102119]
[95]
Wilke MH. Multiresistant bacteria and current therapy - the economical side of the story. Eur J Med Res 2010; 15(12): 571-6.
[http://dx.doi.org/10.1186/2047-783X-15-12-571] [PMID: 21163732]
[96]
Pathak A, Marothi Y, Kekre V, Mahadik K, Macaden R, Lundborg CS. High prevalence of extended-spectrum β-lactamase-producing pathogens: Results of a surveillance study in two hospitals in Ujjain, India. Infect Drug Resist 2012; 5: 65-73.
[http://dx.doi.org/10.2147/IDR.S30043] [PMID: 22570555]
[97]
Tafur JD, Torres JA, Villegas MV. Mecanismos de resistencia a los antibióticos en bacterias Gram negativas. Asoc Colomb Infectol 2008; 12(3): 217-26.
[98]
Silver LL. Challenges of antibacterial discovery. Clin Microbiol Rev 2011; 24(1): 71-109.
[http://dx.doi.org/10.1128/CMR.00030-10] [PMID: 21233508]
[99]
Lazdunski A, Murgier M, Lazdunski C. Evidence for an aminoendopeptidase localized near the cell surface of Escherichia coli. Regulation of synthesis by inorganic phosphate. Eur J Biochem 1975; 60(2): 349-55.
[http://dx.doi.org/10.1111/j.1432-1033.1975.tb21009.x] [PMID: 1107039]
[100]
Gottesman S. Proteases and their targets in Escherichia coli. Annu Rev Genet 1996; 30(1): 465-506.
[http://dx.doi.org/10.1146/annurev.genet.30.1.465] [PMID: 8982462]
[101]
Foglino M, Gharbi S, Lazdunski A. Nucleotide sequence of the pepN gene encoding aminopeptidase N of Escherichia coli. Gene 1986; 49(3): 303-9.
[http://dx.doi.org/10.1016/0378-1119(86)90366-5] [PMID: 2436977]
[102]
Addlagatta A, Gay L, Matthews BW. Structure of aminopeptidase N from Escherichia coli suggests a compartmentalized, gated active site. Proc Natl Acad Sci USA 2006; 103(36): 13339-44.
[http://dx.doi.org/10.1073/pnas.0606167103] [PMID: 16938892]
[103]
Golich FC, Han M, Crowder MW. Over-expression, purification, and characterization of aminopeptidase N from Escherichia coli. Protein Expr Purif 2006; 47(2): 634-9.
[http://dx.doi.org/10.1016/j.pep.2005.11.012] [PMID: 16380266]
[104]
McCaman MT, Villarejo MR. Structured and catalytic properties of peptidase N from Escherichia coli K-12. Arch Biochem Biophys 1982; 213(2): 384-94.
[http://dx.doi.org/10.1016/0003-9861(82)90564-1] [PMID: 7041825]
[105]
Chandu D, Kumar A, Nandi D. PepN, the major Suc-LLVY-AMC-hydrolyzing enzyme in Escherichia coli, displays functional similarity with downstream processing enzymes in Archaea and eukarya. Implications in cytosolic protein degradation. J Biol Chem 2003; 278(8): 5548-56.
[http://dx.doi.org/10.1074/jbc.M207926200] [PMID: 12482750]
[106]
González-Bacerio J, Fando R, del Monte-Martínez A, Charli J-L, Chávez ML. Plasmodium falciparum M1-aminopeptidase: A promising target for the development of antimalarials. Curr Drug Targets 2014; 15(12): 1144-65.
[http://dx.doi.org/10.2174/1389450115666141024115641] [PMID: 25341419]
[107]
Méndez Y, Pérez-Labrada K, González-Bacerio J, et al. Combinatorial multicomponent access to natural-products-inspired peptidomimetics: Discovery of selective inhibitors of microbial metallo-aminopeptidases. ChemMedChem 2014; 9(10): 2351-9.
[http://dx.doi.org/10.1002/cmdc.201402140] [PMID: 24989844]
[108]
Méndez Y, De Armas G, Pérez I, et al. Discovery of potent and selective inhibitors of the Escherichia coli M1-aminopeptidase via multicomponent solid-phase synthesis of tetrazole-peptidomimetics. Eur J Med Chem 2019; 163: 481-99.
[http://dx.doi.org/10.1016/j.ejmech.2018.11.074] [PMID: 30544037]
[109]
Varela AC, Pérez I, De Armas G, et al. Structure-activity relationship of the inhibition of M1-aminopeptidases from Escherichia coli (ePepN) and Plasmodium falciparum (PfA-M1) by bestatin-derived peptidomimetics. Rev Cub Cien Biol 2019; 7(1): 1-21.
[110]
Ganji RJ, Reddi R, Gumpena R, et al. Structural basis for the inhibition of M1 family aminopeptidases by the natural product actinonin: Crystal structure in complex with E. coli aminopeptidase N. Protein Sci 2015; 24(5): 823-31.
[http://dx.doi.org/10.1002/pro.2653] [PMID: 25644575]
[111]
Kumar A, Bhosale M, Reddy S, Srinivasan N, Nandi D. Importance of non-conserved distal carboxyl terminal amino acids in two peptidases belonging to the M1 family: Thermoplasma acidophilum Tricorn interacting factor F2 and Escherichia coli Peptidase N. Biochimie 2009; 91(9): 1145-55.
[http://dx.doi.org/10.1016/j.biochi.2009.06.002] [PMID: 19527767]
[112]
Gumpena R, Kishor C, Ganji RJ, Jain N, Addlagatta A. Glu121-Lys319 salt bridge between catalytic and N-terminal domains is pivotal for the activity and stability of Escherichia coli aminopeptidase N. Protein Sci 2012; 21(5): 727-36.
[http://dx.doi.org/10.1002/pro.2060] [PMID: 22411732]
[113]
Salomon E, Schmitt M, Marapaka AK, et al. Aminobenzosuberone scaffold as a modular chemical tool for the inhibition of therapeutically relevant M1 aminopeptidases. Molecules 2018; 23(10): 2607.
[http://dx.doi.org/10.3390/molecules23102607] [PMID: 30314342]
[114]
Gharbi S, Belaich A, Murgier M, Lazdunski A. Multiple controls exerted on in vivo expression of the pepN gene in Escherichia coli: Studies with pepN-lacZ operon and protein fusion strains. J Bacteriol 1985; 163(3): 1191-5.
[http://dx.doi.org/10.1128/jb.163.3.1191-1195.1985] [PMID: 2863254]
[115]
Bhosale M, Kumar A, Das M, Bhaskarla C, Agarwal V, Nandi D. Catalytic activity of Peptidase N is required for adaptation of Escherichia coli to nutritional downshift and high temperature stress. Microbiol Res 2013; 168(1): 56-64.
[http://dx.doi.org/10.1016/j.micres.2012.06.003] [PMID: 22766257]
[116]
Kazakov T, Vondenhoff GH, Datsenko KA, et al. Escherichia coli peptidase A, B, or N can process translation inhibitor microcin C. J Bacteriol 2008; 190(7): 2607-10.
[http://dx.doi.org/10.1128/JB.01956-07] [PMID: 18223070]
[117]
Onohara Y, Nakajima Y, Ito K, et al. Crystallization and preliminary X-ray characterization of aminopeptidase N from Escherichia coli. Acta Crystallogr Sect F Struct Biol Cryst Commun 2006; 62(Pt 7): 699-701.
[http://dx.doi.org/10.1107/S1744309106021567] [PMID: 16820698]
[118]
Chappelet-Tordo D, Lazdunski C, Murgier M, Lazdunski A. Aminopeptidase N from Escherichia coli: Ionizable active-center groups and substrate specificity. Eur J Biochem 1977; 81(2): 293-305.
[http://dx.doi.org/10.1111/j.1432-1033.1977.tb11952.x] [PMID: 340221]
[119]
Lazdunski C, Busuttil J, Lazdunski A. Purification and properties of a periplasmic aminoendopeptidase from Escherichia coli. Eur J Biochem 1975; 60(2): 363-9.
[http://dx.doi.org/10.1111/j.1432-1033.1975.tb21011.x] [PMID: 1271]
[120]
Yoshimoto T, Tamesa Y, Gushi K, Murayama N, Tsuru D. An aminopeptidase N from Escherichia coli HB1010: Purification and demonstration that the enzyme possesses arylamidase and peptidase activities. Agric Biol Chem 1988; 52(1): 217-25.
[121]
González-Bacerio J, Osuna J, Ponce A, et al. High-level expression in Escherichia coli, purification and kinetic characterization of Plasmodium falciparum M1-aminopeptidase. Protein Expr Purif 2014; 104: 103-14.
[http://dx.doi.org/10.1016/j.pep.2014.08.002] [PMID: 25123643]
[122]
Yang KW, Golich FC, Sigdel TK, Crowder MW. Phosphinate, sulfonate, and sulfonamidate dipeptides as potential inhibitors of Escherichia coli aminopeptidase N. Bioorg Med Chem Lett 2005; 15(23): 5150-3.
[http://dx.doi.org/10.1016/j.bmcl.2005.08.055] [PMID: 16168644]
[123]
Chen H, Roques BP, Fournié-Zaluski MC. Design of the first highly potent and selective aminopeptidase N (EC 3.4.11.2) inhibitor. Bioorg Med Chem Lett 1999; 9(11): 1511-6.
[http://dx.doi.org/10.1016/S0960-894X(99)00219-X] [PMID: 10386926]
[124]
Peng G, McEwen AG, Olieric V, et al. Insight into the remarkable affinity and selectivity of the aminobenzosuberone scaffold for the M1 aminopeptidases family based on structure analysis. Proteins 2017; 85(8): 1413-21.
[http://dx.doi.org/10.1002/prot.25301] [PMID: 28383176]
[125]
Umezawa H, Aoyagi T, Suda H, Hamada M, Takeuchi T. Bestatin, an inhibitor of aminopeptidase B, produced by actinomycetes. J Antibiot (Tokyo) 1976; 29(1): 97-9.
[http://dx.doi.org/10.7164/antibiotics.29.97] [PMID: 931798]
[126]
Suda H, Takita T, Aoyagi T, Umezawa H. The chemical synthesis of bestatin. J Antibiot (Tokyo) 1976; 29(5): 600-1.
[http://dx.doi.org/10.7164/antibiotics.29.600] [PMID: 956051]
[127]
Nishizawa R, Saino T, Takita T, Suda H, Aoyagi T, Umezawa H. Synthesis and structure-activity relationships of bestatin analogues, inhibitors of aminopeptidase B. J Med Chem 1977; 20(4): 510-5.
[http://dx.doi.org/10.1021/jm00214a010] [PMID: 850237]
[128]
Scornik OA, Botbol V. Bestatin as an experimental tool in mammals. Curr Drug Metab 2001; 2(1): 67-85.
[http://dx.doi.org/10.2174/1389200013338748] [PMID: 11465152]
[129]
Xu W, Li Q. Progress in the development of aminopeptidase N (APN/CD13) inhibitors. Curr Med Chem Anticancer Agents 2005; 5(3): 281-301.
[http://dx.doi.org/10.2174/1568011053765949] [PMID: 15992355]
[130]
Wilkes SH, Prescott JM. The slow, tight binding of bestatin and amastatin to aminopeptidases. J Biol Chem 1985; 260(24): 13154-62.
[http://dx.doi.org/10.1016/S0021-9258(17)38851-8] [PMID: 2865258]
[131]
Fournié-Zaluski MC, Poras H, Roques BP, Nakajima Y, Ito K, Yoshimoto T. Structure of aminopeptidase N from Escherichia coli complexed with the transition-state analogue aminophosphinic inhibitor PL250. Acta Crystallogr D Biol Crystallogr 2009; 65(Pt 8): 814-22.
[http://dx.doi.org/10.1107/S090744490901779X] [PMID: 19622865]
[132]
Labbé S, Grenier D, Plamondon P, Uitto VJ, Mayrand D. Effects of dipeptide bestatin on Porphyromonas gingivalis and epithelial cells. J Periodontol 2001; 72(6): 714-21.
[http://dx.doi.org/10.1902/jop.2001.72.6.714] [PMID: 11453232]
[133]
Harbut MB, Velmourougane G, Reiss G, Chandramohanadas R, Greenbaum DC. Development of bestatin-based activity-based probes for metallo-aminopeptidases. Bioorg Med Chem Lett 2008; 18(22): 5932-6.
[http://dx.doi.org/10.1016/j.bmcl.2008.09.021] [PMID: 18823778]
[134]
Suzuki H, Kamatani S, Kumagai H. Purification and characterization of aminopeptidase B from Escherichia coli K-12. Biosci Biotechnol Biochem 2001; 65(7): 1549-58.
[http://dx.doi.org/10.1271/bbb.65.1549] [PMID: 11515538]
[135]
Bhosale M, Pande S, Kumar A, Kairamkonda S, Nandi D. Characterization of two M17 family members in Escherichia coli, Peptidase A and Peptidase B. Biochem Biophys Res Commun 2010; 395(1): 76-81.
[http://dx.doi.org/10.1016/j.bbrc.2010.03.142] [PMID: 20350528]
[136]
Sträter N, Sherratt DJ, Colloms SD. X-ray structure of aminopeptidase A from Escherichia coli and a model for the nucleoprotein complex in Xer site-specific recombination. EMBO J 1999; 18(16): 4513-22.
[http://dx.doi.org/10.1093/emboj/18.16.4513] [PMID: 10449417]
[137]
Charlier D, Kholti A, Huysveld N, et al. Mutational analysis of Escherichia coli PepA, a multifunctional DNA-binding aminopeptidase. J Mol Biol 2000; 302(2): 411-26.
[http://dx.doi.org/10.1006/jmbi.2000.4067] [PMID: 10970742]
[138]
Reijns M, Lu Y, Leach S, Colloms SD. Mutagenesis of PepA suggests a new model for the Xer/cer synaptic complex. Mol Microbiol 2005; 57(4): 927-41.
[http://dx.doi.org/10.1111/j.1365-2958.2005.04716.x] [PMID: 16091035]
[139]
Minh PN, Devroede N, Massant J, Maes D, Charlier D. Insights into the architecture and stoichiometry of Escherichia coli PepA*DNA complexes involved in transcriptional control and site-specific DNA recombination by atomic force microscopy. Nucleic Acids Res 2009; 37(5): 1463-76.
[http://dx.doi.org/10.1093/nar/gkn1078] [PMID: 19136463]
[140]
Nguyen Le Minh P, Nadal M, Charlier D. The trigger enzyme PepA (aminopeptidase A) of Escherichia coli, a transcriptional repressor that generates positive supercoiling. FEBS Lett 2016; 590(12): 1816-25.
[http://dx.doi.org/10.1002/1873-3468.12224] [PMID: 27213286]
[141]
Baba T, Ara T, Hasegawa M, et al. Construction of Escherichia coli K-12 in frame, single-gene knockout mutants: The Keio collection. Mol Syst Biol 2006; 2: 2006.0008.
[http://dx.doi.org/10.1038/msb4100050]
[142]
Charlier D, Hassanzadeh G, Kholti A, Gigot D, Piérard A, Glansdorff N. carP, involved in pyrimidine regulation of the Escherichia coli carbamoylphosphate synthetase operon encodes a sequence-specific DNA-binding protein identical to XerB and PepA, also required for resolution of ColEI multimers. J Mol Biol 1995; 250(4): 392-406.
[http://dx.doi.org/10.1006/jmbi.1995.0385] [PMID: 7616564]
[143]
Stirling CJ, Colloms SD, Collins JF, Szatmari G, Sherratt DJ. xerB, an Escherichia coli gene required for plasmid ColE1 site-specific recombination, is identical to pepA, encoding aminopeptidase A, a protein with substantial similarity to bovine lens leucine aminopeptidase. EMBO J 1989; 8(5): 1623-7.
[http://dx.doi.org/10.1002/j.1460-2075.1989.tb03547.x] [PMID: 2670557]
[144]
McCulloch R, Burke ME, Sherratt DJ. Peptidase activity of Escherichia coli aminopeptidase A is not required for its role in Xer site-specific recombination. Mol Microbiol 1994; 12(2): 241-51.
[http://dx.doi.org/10.1111/j.1365-2958.1994.tb01013.x] [PMID: 8057849]
[145]
Miller CG, Schwartz G. Peptidase-deficient mutants of Escherichia coli. J Bacteriol 1978; 135(2): 603-11.
[http://dx.doi.org/10.1128/jb.135.2.603-611.1978] [PMID: 355237]
[146]
Suzuki H, Hashimoto W, Kumagai H. Escherichia coli K-12 can utilize an exogenous γ-glutamyl peptide as an amino acid source, for which γ-glutamyltranspeptidase is essential. J Bacteriol 1993; 175(18): 6038-40.
[http://dx.doi.org/10.1128/jb.175.18.6038-6040.1993] [PMID: 8104180]
[147]
Suzuki H, Hashimoto W, Kumagai H. Glutathione metabolism in Escherichia coli. J Mol Catal, B Enzym 1999; 6(3): 175-84.
[http://dx.doi.org/10.1016/S1381-1177(98)00116-7]
[148]
Suzuki H, Kamatani S, Kim E-S, Kumagai H, Aminopeptidase A. B and N and dipeptidase D are the four cysteinylglycinases of Escherichia coli K-12 J Bacteriol 2001; 183(4): 1489-90.
[http://dx.doi.org/10.1128/JB.183.4.1489-1490.2001] [PMID: 11157967]
[149]
Basten DEJW, Visser J, Schaap PJ. Lysine aminopeptidase of Aspergillus niger. Microbiology 2001; 147(Pt 8): 2045-50.
[http://dx.doi.org/10.1099/00221287-147-8-2045] [PMID: 11495983]
[150]
Mathew Z, Knox TM, Miller CG. Salmonella enterica serovar typhimurium peptidase B is a leucyl aminopeptidase with specificity for acidic amino acids. J Bacteriol 2000; 182(12): 3383-93.
[http://dx.doi.org/10.1128/JB.182.12.3383-3393.2000] [PMID: 10852868]
[151]
Silver S. Transport of inorganic cationsEscherichia coli and salmonella: Cellular and molecular biology. 2nd ed. Washington, DC: American Society for Microbiology 1996; vol. 1: pp. 1091-10.
[152]
WHO. 2011/2012 Tuberculosis global facts Available from: http://www.who.int/tb/publications/2011/factsheet_tb_2011.pdf
[153]
Stokstad E. Infectious disease. Drug-resistant TB on the rise. Science 2000; 287(5462): 2391.
[http://dx.doi.org/10.1126/science.287.5462.2391a] [PMID: 10766610]
[154]
WHO. Global tuberculosis report Available from: http://www.who.int/tb/publications/global_report/en/
[155]
Ducati RG, Ruffino-Netto A, Basso LA, Santos DS. The resumption of consumption -- a review on tuberculosis. Mem Inst Oswaldo Cruz 2006; 101(7): 697-714.
[http://dx.doi.org/10.1590/S0074-02762006000700001] [PMID: 17160276]
[156]
Schwander S, Dheda K. Human lung immunity against Mycobacterium tuberculosis: insights into pathogenesis and protection. Am J Respir Crit Care Med 2011; 183(6): 696-707.
[http://dx.doi.org/10.1164/rccm.201006-0963PP] [PMID: 21075901]
[157]
Jamwal SV, Mehrotra P, Singh A, Siddiqui Z, Basu A, Rao KVS. Mycobacterial escape from macrophage phagosomes to the cytoplasm represents an alternate adaptation mechanism. Sci Rep 2016; 6(1): 23089.
[http://dx.doi.org/10.1038/srep23089] [PMID: 26980157]
[158]
Ernst JD. The immunological life cycle of tuberculosis. Nat Rev Immunol 2012; 12(8): 581-91.
[http://dx.doi.org/10.1038/nri3259] [PMID: 22790178]
[159]
McKinney JD, Höner zu Bentrup K, Muñoz-Elías EJ, et al. Persistence of Mycobacterium tuberculosis in macrophages and mice requires the glyoxylate shunt enzyme isocitrate lyase. Nature 2000; 406(6797): 735-8.
[http://dx.doi.org/10.1038/35021074] [PMID: 10963599]
[160]
Correa AF, Bastos IMD, Neves D, Kipnis A, Junqueira-Kipnis AP, de Santana JM. The activity of a hexameric M17 metallo-aminopeptidase is associated with survival of Mycobacterium tuberculosis. Front Microbiol 2017; 8: 504.
[http://dx.doi.org/10.3389/fmicb.2017.00504] [PMID: 28396657]
[161]
Singh AK, Singh R, Tomar D, Pandya CD, Singh R. The leucine aminopeptidase of Staphylococcus aureus is secreted and contributes to biofilm formation. Int J Infect Dis 2012; 16(5): e375-81.
[http://dx.doi.org/10.1016/j.ijid.2012.01.009] [PMID: 22410279]
[162]
Aboge GO, Cao S, Terkawi MA, et al. Molecular characterization of Babesia bovis M17 leucine aminopeptidase and inhibition of Babesia growth by bestatin. J Parasitol 2015; 101(5): 536-41.
[http://dx.doi.org/10.1645/15-745.1] [PMID: 26057618]
[163]
Vandal OH, Pierini LM, Schnappinger D, Nathan CF, Ehrt S. A membrane protein preserves intrabacterial pH in intraphagosomal Mycobacterium tuberculosis. Nat Med 2008; 14(8): 849-54.
[http://dx.doi.org/10.1038/nm.1795] [PMID: 18641659]
[164]
Kehl-Fie TE, Chitayat S, Hood MI, et al. Nutrient metal sequestration by calprotectin inhibits bacterial superoxide defense, enhancing neutrophil killing of Staphylococcus aureus. Cell Host Microbe 2011; 10(2): 158-64.
[http://dx.doi.org/10.1016/j.chom.2011.07.004] [PMID: 21843872]
[165]
Hood MI, Skaar EP. Nutritional immunity: Transition metals at the pathogen-host interface. Nat Rev Microbiol 2012; 10(8): 525-37.
[http://dx.doi.org/10.1038/nrmicro2836] [PMID: 22796883]
[166]
Olaleye O, Raghunand TR, Bhat S, et al. Methionine aminopeptidases from Mycobacterium tuberculosis as novel antimycobacterial targets. Chem Biol 2010; 17(1): 86-97.
[http://dx.doi.org/10.1016/j.chembiol.2009.12.014] [PMID: 20142044]
[167]
Narayanan SS, Nampoothiri KM. Biochemical characterization of recombinant methionine aminopeptidases (MAPs) from Mycobacterium tuberculosis H37Rv. Mol Cell Biochem 2012; 365(1-2): 191-202.
[http://dx.doi.org/10.1007/s11010-012-1260-8] [PMID: 22466806]
[168]
Zhang X, Chen S, Hu Z, Zhang L, Wang H. Expression and characterization of two functional methionine aminopeptidases from Mycobacterium tuberculosis H37Rv. Curr Microbiol 2009; 59(5): 520-5.
[http://dx.doi.org/10.1007/s00284-009-9470-3] [PMID: 19688379]
[169]
Addlagatta A, Quillin ML, Omotoso O, Liu JO, Matthews BW. Identification of an SH3-binding motif in a new class of methionine aminopeptidases from Mycobacterium tuberculosis suggests a mode of interaction with the ribosome. Biochemistry 2005; 44(19): 7166-74.
[http://dx.doi.org/10.1021/bi0501176] [PMID: 15882055]
[170]
Mayer BJ. SH3 domains: Complexity in moderation. J Cell Sci 2001; 114(Pt 7): 1253-63.
[http://dx.doi.org/10.1242/jcs.114.7.1253] [PMID: 11256992]
[171]
Renzoni DA, Pugh DJ, Siligardi G, et al. Structural and thermodynamic characterization of the interaction of the SH3 domain from Fyn with the proline-rich binding site on the p85 subunit of PI3-kinase. Biochemistry 1996; 35(49): 15646-53.
[http://dx.doi.org/10.1021/bi9620969] [PMID: 8961927]
[172]
Olaleye OA, Bishai WR, Liu JO. Targeting the role of N-terminal methionine processing enzymes in Mycobacterium tuberculosis. Tuberculosis (Edinb) 2009; 89(Suppl. 1): S55-9.
[http://dx.doi.org/10.1016/S1472-9792(09)70013-7] [PMID: 20006307]
[173]
Kerwar SS, Weissbach H, Glenner GG. An aminopeptidase activity associated with brain ribosomes. Arch Biochem Biophys 1971; 143(1): 336-7.
[http://dx.doi.org/10.1016/0003-9861(71)90215-3] [PMID: 5561749]
[174]
Luo QL, Li JY, Liu ZY, et al. Discovery and structural modification of inhibitors of methionine aminopeptidases from Escherichia coli and Saccharomyces cerevisiae. J Med Chem 2003; 46(13): 2631-40.
[http://dx.doi.org/10.1021/jm0300532] [PMID: 12801227]
[175]
Oefner C, Douangamath A, D’Arcy A, et al. The 1.15A crystal structure of the Staphylococcus aureus methionyl-aminopeptidase and complexes with triazole based inhibitors. J Mol Biol 2003; 332(1): 13-21.
[http://dx.doi.org/10.1016/S0022-2836(03)00862-3] [PMID: 12946343]
[176]
Cui YM, Huang QQ, Xu J, et al. Identification of potent type I MetAP inhibitors by simple bioisosteric replacement. Part 1: Synthesis and preliminary SAR studies of thiazole-4-carboxylic acid thiazol-2-ylamide derivatives. Bioorg Med Chem Lett 2005; 15(16): 3732-6.
[http://dx.doi.org/10.1016/j.bmcl.2005.05.055] [PMID: 15993057]
[177]
Hu X, Addlagatta A, Matthews BW, Liu JO. Identification of pyridinylpyrimidines as inhibitors of human methionine aminopeptidases. Angew Chem Int Ed 2006; 45(23): 3772-5.
[http://dx.doi.org/10.1002/anie.200600757] [PMID: 16724298]
[178]
Olaleye O, Raghunand TR, Bhat S, et al. Characterization of clioquinol and analogues as novel inhibitors of methionine aminopeptidases from Mycobacterium tuberculosis. Tuberculosis (Edinb) 2011; 91(Suppl. 1): S61-5.
[http://dx.doi.org/10.1016/j.tube.2011.10.012] [PMID: 22115541]
[179]
Bhat S, Olaleye O, Meyer KJ, Shi W, Zhang Y, Liu JO. Analogs of N′-hydroxy-N-(4H,5H-naphtho[1,2-d]thiazol-2-yl)methanimida-mide inhibit Mycobacterium tuberculosis methionine aminopeptidases. Bioorg Med Chem 2012; 20(14): 4507-13.
[http://dx.doi.org/10.1016/j.bmc.2012.05.022] [PMID: 22704656]
[180]
Kishor C, Gumpena R, Reddi R, Addlagatta A. Structural studies of Enterococcus faecalis methionine aminopeptidase and design of microbe specific 2,2′-bipyridine based inhibitors. MedChemComm 2012; 3(11): 1406-12.
[http://dx.doi.org/10.1039/c2md20096a]
[181]
Krátký M, Vinšová J, Novotná E, et al. Salicylanilide derivatives block Mycobacterium tuberculosis through inhibition of isocitrate lyase and methionine aminopeptidase. Tuberculosis (Edinb) 2012; 92(5): 434-9.
[http://dx.doi.org/10.1016/j.tube.2012.06.001] [PMID: 22765970]
[182]
Xu W, Lu JP, Ye QZ. Structural analysis of bengamide derivatives as inhibitors of methionine aminopeptidases. J Med Chem 2012; 55(18): 8021-7.
[http://dx.doi.org/10.1021/jm3008695] [PMID: 22913487]
[183]
John SF, Aniemeke E, Ha NP, et al. Characterization of 2-hydroxy-1-naphthaldehyde isonicotinoyl hydrazone as a novel inhibitor of methionine aminopeptidases from Mycobacterium tuberculosis. Tuberculosis (Edinb) 2016; 101S: S73-7.
[http://dx.doi.org/10.1016/j.tube.2016.09.025] [PMID: 27856197]
[184]
Lu JP, Ye QZ. Expression and characterization of Mycobacterium tuberculosis methionine aminopeptidase type 1a. Bioorg Med Chem Lett 2010; 20(9): 2776-9.
[http://dx.doi.org/10.1016/j.bmcl.2010.03.067] [PMID: 20363127]
[185]
Lu JP, Chai SC, Ye QZ. Catalysis and inhibition of Mycobacterium tuberculosis methionine aminopeptidase. J Med Chem 2010; 53(3): 1329-37.
[http://dx.doi.org/10.1021/jm901624n] [PMID: 20038112]
[186]
Addlagatta A, Matthews BW. Structure of the angiogenesis inhibitor ovalicin bound to its noncognate target, human Type 1 methionine aminopeptidase. Protein Sci 2006; 15(8): 1842-8.
[http://dx.doi.org/10.1110/ps.062278006] [PMID: 16823043]
[187]
Hu X, Addlagatta A, Lu J, Matthews BW, Liu JO. Elucidation of the function of type 1 human methionine aminopeptidase during cell cycle progression. Proc Natl Acad Sci USA 2006; 103(48): 18148-53.
[http://dx.doi.org/10.1073/pnas.0608389103] [PMID: 17114291]
[188]
Lu JP, Yuan X-H, Ye Q-Z. Structural analysis of inhibition of Mycobacterium tuberculosis methionine aminopeptidase by bengamide derivatives. Eur J Med Chem 2012; 47(1): 479-84.
[http://dx.doi.org/10.1016/j.ejmech.2011.11.017] [PMID: 22118830]
[189]
Sander C, Schneider R. Database of homology-derived protein structures and the structural meaning of sequence alignment. Proteins 1991; 9(1): 56-68.
[http://dx.doi.org/10.1002/prot.340090107] [PMID: 2017436]
[190]
Pavelka A, Chovancova E, Damborsky J. HotSpot Wizard: A web server for identification of hot spots in protein engineering. Nucleic Acids Res 2009; 37(Web Server issue): W376-83.
[http://dx.doi.org/10.1093/nar/gkp410] [PMID: 19465397]
[191]
Carroll RK, Veillard F, Gagne DT, et al. The Staphylococcus aureus leucine aminopeptidase is localized to the bacterial cytosol and demonstrates a broad substrate range that extends beyond leucine. Biol Chem 2013; 394(6): 791-803.
[http://dx.doi.org/10.1515/hsz-2012-0308] [PMID: 23241672]
[192]
Coulter SN, Schwan WR, Ng EY, et al. Staphylococcus aureus genetic loci impacting growth and survival in multiple infection environments. Mol Microbiol 1998; 30(2): 393-404.
[http://dx.doi.org/10.1046/j.1365-2958.1998.01075.x] [PMID: 9791183]
[193]
Rice K, Peralta R, Bast D, de Azavedo J, McGavin MJ. Description of staphylococcus serine protease (ssp) operon in Staphylococcus aureus and nonpolar inactivation of sspA-encoded serine protease. Infect Immun 2001; 69(1): 159-69.
[http://dx.doi.org/10.1128/IAI.69.1.159-169.2001] [PMID: 11119502]
[194]
Shaw L, Golonka E, Potempa J, Foster SJ. The role and regulation of the extracellular proteases of Staphylococcus aureus. Microbiology 2004; 150(Pt 1): 217-28.
[http://dx.doi.org/10.1099/mic.0.26634-0] [PMID: 14702415]
[195]
Kantyka T, Shaw LN, Potempa J. Papain-like proteases of Staphylococcus aureus Cysteine proteases of pathogenic organisms Adv Exp Med Biol. Boston: Springer 2011; Vol. 712: pp. 1-14.
[http://dx.doi.org/10.1007/978-1-4419-8414-2_1]
[196]
Drinkwater N, Lee J, Yang W, Malcolm TR, McGowan S. M1 aminopeptidases as drug targets: Broad applications or therapeutic niche? FEBS J 2017; 284(10): 1473-88.
[http://dx.doi.org/10.1111/febs.14009] [PMID: 28075056]
[197]
Masip L, Veeravalli K, Georgiou G. The many faces of glutathione in bacteria. Antioxid Redox Signal 2006; 8(5-6): 753-62.
[http://dx.doi.org/10.1089/ars.2006.8.753] [PMID: 16771667]
[198]
Soutourina O, Poupel O, Coppée JY, Danchin A, Msadek T, Martin-Verstraete I. CymR, the master regulator of cysteine metabolism in Staphylococcus aureus, controls host sulphur source utilization and plays a role in biofilm formation. Mol Microbiol 2009; 73(2): 194-211.
[http://dx.doi.org/10.1111/j.1365-2958.2009.06760.x] [PMID: 19508281]
[199]
Newton GL, Rawat M, La Clair JJ, et al. Bacillithiol is an antioxidant thiol produced in Bacilli. Nat Chem Biol 2009; 5(9): 625-7.
[http://dx.doi.org/10.1038/nchembio.189] [PMID: 19578333]
[200]
Kasperkiewicz P, Gajda AD, Drąg M. Current and prospective applications of non-proteinogenic amino acids in profiling of proteases substrate specificity. Biol Chem 2012; 393(9): 843-51.
[http://dx.doi.org/10.1515/hsz-2012-0167] [PMID: 22944686]
[201]
Cappiello M, Lazzarotti A, Buono F, et al. New role for leucyl aminopeptidase in glutathione turnover. Biochem J 2004; 378(Pt 1): 35-44.
[http://dx.doi.org/10.1042/bj20031336] [PMID: 14583094]
[202]
Kapatral V, Zago A, Kamath S, Chugani S. Pseudomonas Encyclopedia of microbiology. San Diego: Academic Press 2000; Vol. 3: p. 876.
[203]
Davies JC. Pseudomonas aeruginosa in cystic fibrosis: Pathogenesis and persistence. Paediatr Respir Rev 2002; 3(2): 128-34.
[http://dx.doi.org/10.1016/S1526-0550(02)00003-3] [PMID: 12297059]
[204]
Stewart PS, Costerton JW. Antibiotic resistance of bacteria in biofilms. Lancet 2001; 358(9276): 135-8.
[http://dx.doi.org/10.1016/S0140-6736(01)05321-1] [PMID: 11463434]
[205]
Costerton JW, Stewart PS, Greenberg EP. Bacterial biofilms: A common cause of persistent infections. Science 1999; 284(5418): 1318-22.
[http://dx.doi.org/10.1126/science.284.5418.1318] [PMID: 10334980]
[206]
Mulet X, Maciá MD, Mena A, Juan C, Pérez JL, Oliver A. Azithromycin in Pseudomonas aeruginosa biofilms: Bactericidal activity and selection of nfxB mutants. Antimicrob Agents Chemother 2009; 53(4): 1552-60.
[http://dx.doi.org/10.1128/AAC.01264-08] [PMID: 19188376]
[207]
Woolwine SC, Sprinkle AB, Wozniak DJ. Loss of Pseudomonas aeruginosa PhpA aminopeptidase activity results in increased algD transcription. J Bacteriol 2001; 183(15): 4674-9.
[http://dx.doi.org/10.1128/JB.183.15.4674-4679.2001] [PMID: 11443106]
[208]
Hentzer M, Teitzel GM, Balzer GJ, et al. Alginate overproduction affects Pseudomonas aeruginosa biofilm structure and function. J Bacteriol 2001; 183(18): 5395-401.
[http://dx.doi.org/10.1128/JB.183.18.5395-5401.2001] [PMID: 11514525]
[209]
Simonson LG, Goodman CH, Bial JJ, Morton HE. Quantitative relationship of Treponema denticola to severity of periodontal disease. Infect Immun 1988; 56(4): 726-8.
[http://dx.doi.org/10.1128/iai.56.4.726-728.1988] [PMID: 3346072]
[210]
Sela MN. Role of Treponema denticola in periodontal diseases. Crit Rev Oral Biol Med 2001; 12(5): 399-413.
[http://dx.doi.org/10.1177/10454411010120050301] [PMID: 12002822]
[211]
Holt SC, Ebersole JL. Porphyromonas gingivalis, Treponema denticola, and Tannerella forsythia: The “red complex”, a prototype polybacterial pathogenic consortium in periodontitis. Periodontol 2000 2005; 38(1): 72-122.
[http://dx.doi.org/10.1111/j.1600-0757.2005.00113.x] [PMID: 15853938]
[212]
Aimetti M, Romano F, Nessi F. Microbiologic analysis of periodontal pockets and carotid atheromatous plaques in advanced chronic periodontitis patients. J Periodontol 2007; 78(9): 1718-23.
[http://dx.doi.org/10.1902/jop.2007.060473] [PMID: 17760541]
[213]
Morhart RE, Mata LJ, Sinskey AJ, Harris RS. A microbiological and biochemical study of gingival crevice debris obtained from Guatemalan Mayan Indians. J Periodontol 1970; 41(11): 644-9.
[http://dx.doi.org/10.1902/jop.1970.41.11.644] [PMID: 4320450]
[214]
Horowitz A, Folke LE. Hydrogen sulfide production in the periodontal environment. J Periodontol 1973; 44(7): 390-5.
[http://dx.doi.org/10.1902/jop.1973.44.7.390] [PMID: 4514569]
[215]
Chu L, Lai Y, Xu X, et al. A 52-kDa leucyl aminopeptidase from treponema denticola is a cysteinylglycinase that mediates the second step of glutathione metabolism. J Biol Chem 2008; 283(28): 19351-8.
[http://dx.doi.org/10.1074/jbc.M801034200] [PMID: 18482986]
[216]
Seshadri R, Myers GS, Tettelin H, et al. Comparison of the genome of the oral pathogen Treponema denticola with other spirochete genomes. Proc Natl Acad Sci USA 2004; 101(15): 5646-51.
[http://dx.doi.org/10.1073/pnas.0307639101] [PMID: 15064399]
[217]
Chu L, Dong Z, Xu X, Cochran DL, Ebersole JL. Role of glutathione metabolism of Treponema denticola in bacterial growth and virulence expression. Infect Immun 2002; 70(3): 1113-20.
[http://dx.doi.org/10.1128/IAI.70.3.1113-1120.2002] [PMID: 11854190]
[218]
Jösch C, Klotz LO, Sies H. Identification of cytosolic leucyl aminopeptidase (EC 3.4.11.1) as the major cysteinylglycine-hydrolysing activity in rat liver. Biol Chem 2003; 384(2): 213-8.
[http://dx.doi.org/10.1515/BC.2003.023] [PMID: 12675513]
[219]
Carlsson J, Larsen JT, Edlund MB. Utilization of glutathione (L-gamma-glutamyl-L-cysteinylglycine) by Fusobacterium nucleatum subspecies nucleatum. Oral Microbiol Immunol 1994; 9(5): 297-300.
[http://dx.doi.org/10.1111/j.1399-302X.1994.tb00074.x] [PMID: 7808772]
[220]
Tang-Larsen J, Claesson R, Edlund MB, Carlsson J. Competition for peptides and amino acids among periodontal bacteria. J Periodontal Res 1995; 30(6): 390-5.
[http://dx.doi.org/10.1111/j.1600-0765.1995.tb01292.x] [PMID: 8544102]
[221]
Smirnova GV, Oktyabrsky ON. Glutathione in bacteria. Biochemistry (Mosc) 2005; 70(11): 1199-211.
[http://dx.doi.org/10.1007/s10541-005-0248-3] [PMID: 16336178]
[222]
Morty RE, Morehead J. Cloning and characterization of a leucyl aminopeptidase from three pathogenic Leishmania species. J Biol Chem 2002; 277(29): 26057-65.
[http://dx.doi.org/10.1074/jbc.M202779200] [PMID: 12006595]
[223]
Dong L, Cheng N, Wang MW, Zhang J, Shu C, Zhu DX. The leucyl aminopeptidase from Helicobacter pylori is an allosteric enzyme. Microbiology 2005; 151(Pt 6): 2017-23.
[http://dx.doi.org/10.1099/mic.0.27767-0] [PMID: 15942008]
[224]
Kreiss C, Blum AL, Malfertheiner P. Peptic ulcer pathogenesis. Curr Opin Gastroenterol 1995; 11: 25-31.
[http://dx.doi.org/10.1097/00001574-199501001-00006]
[225]
Hopkins RJ, Girardi LS, Turney EA. Relationship between Helicobacter pylori eradication and reduced duodenal and gastric ulcer recurrence: A review Gastroenterology 1996; 110(4): 1244-52.
[http://dx.doi.org/10.1053/gast.1996.v110.pm8613015] [PMID: 8613015]
[226]
Cover TL, Blaser MJ. Helicobacter pylori infection, a paradigm for chronic mucosal inflammation: Pathogenesis and implications for eradication and prevention. Adv Intern Med 1996; 41: 85-117.
[PMID: 8903587]
[227]
Malfertheiner P, Mégraud F, O’Morain C, et al. European Helicobacter Pylori Study Group (EHPSG). Current concepts in the management of Helicobacter pylori infection--the Maastricht 2-2000 Consensus Report. Aliment Pharmacol Ther 2002; 16(2): 167-80.
[http://dx.doi.org/10.1046/j.1365-2036.2002.01169.x] [PMID: 11860399]
[228]
Björkholm B, Sjölund M, Falk PG, Berg OG, Engstrand L, Andersson DI. Mutation frequency and biological cost of antibiotic resistance in Helicobacter pylori. Proc Natl Acad Sci USA 2001; 98(25): 14607-12.
[http://dx.doi.org/10.1073/pnas.241517298] [PMID: 11717398]
[229]
Tomb JF, White O, Kerlavage AR, et al. The complete genome sequence of the gastric pathogen Helicobacter pylori. Nature 1997; 388(6642): 539-47.
[http://dx.doi.org/10.1038/41483] [PMID: 9252185]
[230]
Alm RA, Ling LS, Moir DT, et al. Genomic-sequence comparison of two unrelated isolates of the human gastric pathogen Helicobacter pylori. Nature 1999; 397(6715): 176-80.
[http://dx.doi.org/10.1038/16495] [PMID: 9923682]
[231]
Burley SK, David PR, Lipscomb WN. Leucine aminopeptidase: Bestatin inhibition and a model for enzyme-catalyzed peptide hydrolysis. Proc Natl Acad Sci USA 1991; 88(16): 6916-20.
[http://dx.doi.org/10.1073/pnas.88.16.6916] [PMID: 1871107]
[232]
Kale A, Pijning T, Sonke T, Dijkstra BW, Thunnissen AM. Crystal structure of the leucine aminopeptidase from Pseudomonas putida reveals the molecular basis for its enantioselectivity and broad substrate specificity. J Mol Biol 2010; 398(5): 703-14.
[http://dx.doi.org/10.1016/j.jmb.2010.03.042] [PMID: 20359484]
[233]
Qu W, Zhou Y, Shao C, et al. Helicobacter pylori proteins response to nitric oxide stress. J Microbiol 2009; 47(4): 486-93.
[http://dx.doi.org/10.1007/s12275-008-0266-0] [PMID: 19763424]
[234]
Kaakoush NO, Asencio C, Mégraud F, Mendz GL. A redox basis for metronidazole resistance in Helicobacter pylori. Antimicrob Agents Chemother 2009; 53(5): 1884-91.
[http://dx.doi.org/10.1128/AAC.01449-08] [PMID: 19223619]
[235]
Cheng N, Xie JS, Zhang MY, Shu C, Zhu DX. A specific anti-Helicobacter pylori agent NE2001: Synthesis and its effect on the growth of H. pylori. Bioorg Med Chem Lett 2003; 13(16): 2703-7.
[http://dx.doi.org/10.1016/S0960-894X(03)00547-X] [PMID: 12873498]
[236]
Reynolds DJ, Penn CW. Characteristics of Helicobacter pylori growth in a defined medium and determination of its amino acid requirements. Microbiology 1994; 140(Pt 10): 2649-56.
[http://dx.doi.org/10.1099/00221287-140-10-2649] [PMID: 8000535]
[237]
Doig P, de Jonge BL, Alm RA, et al. Helicobacter pylori physiology predicted from genomic comparison of two strains. Microbiol Mol Biol Rev 1999; 63(3): 675-707.
[http://dx.doi.org/10.1128/MMBR.63.3.675-707.1999] [PMID: 10477312]
[238]
Alkhuder K, Meibom KL, Dubail I, Dupuis M, Charbit A. Glutathione provides a source of cysteine essential for intracellular multiplication of Francisella tularensis. PLoS Pathog 2009; 5(1): e1000284
[http://dx.doi.org/10.1371/journal.ppat.1000284] [PMID: 19158962]
[239]
Shibayama K, Wachino J, Arakawa Y, Saidijam M, Rutherford NG, Henderson PJ. Metabolism of glutamine and glutathione via gamma-glutamyltranspeptidase and glutamate transport in Helicobacter pylori: Possible significance in the pathophysiology of the organism. Mol Microbiol 2007; 64(2): 396-406.
[http://dx.doi.org/10.1111/j.1365-2958.2007.05661.x] [PMID: 17381553]
[240]
Gonzales T, Robert-Baudouy J. Bacterial aminopeptidases: Properties and functions. FEMS Microbiol Rev 1996; 18(4): 319-44.
[http://dx.doi.org/10.1111/j.1574-6976.1996.tb00247.x] [PMID: 8703509]
[241]
Ali M, Lopez AL, You YA, et al. The global burden of cholera. Bull World Health Organ 2012; 90(3): 209-218A.
[http://dx.doi.org/10.2471/BLT.11.093427] [PMID: 22461716]
[242]
Charles RC, Ryan ET. Cholera in the 21st century. Curr Opin Infect Dis 2011; 24(5): 472-7.
[http://dx.doi.org/10.1097/QCO.0b013e32834a88af] [PMID: 21799407]
[243]
Conner JG, Teschler JK, Jones CJ, Yildiz FH. Staying alive: Vibrio cholerae’s cycle of environmental survival, transmission, and dissemination. Microbiol Spectr 2016; 4(2): 10.1128.
[http://dx.doi.org/10.1128/microbiolspec.VMBF-0015-2015] [PMID: 27227302]
[244]
Toma C, Honma Y. Cloning and genetic analysis of the Vibrio cholerae aminopeptidase gene. Infect Immun 1996; 64(11): 4495-500.
[http://dx.doi.org/10.1128/iai.64.11.4495-4500.1996] [PMID: 8890197]

Rights & Permissions Print Cite
© 2024 Bentham Science Publishers | Privacy Policy