Role of charged residues of E. coli porins studied using planar lipid bilayers
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1 Role of charged residues of E. coli porins studied using planar lipid bilayers A. Bessonov, K.R. Mahendran, M. Ceccarelli, H. Weingart, M. Winterhalter Mid-Term Review Meeting April, 2008 Marseille, France
2 Background Syrigomycin E (SRE) lipodepsipeptide produced bypseudomonas syringae pv. syringae bacteria MW = 1.2 kda Targets for this toxin - membranes of plants, yeast (Cryptococcus neoformans, Saccharomyces cerevisiae,) and fungi (Candida albicans, Aspergillus fumigatus). Activity against some bacteria (Mycobacterium smegmatis). Biological activity of SRE is governed by the formation of transmembrane pores. Buber et al, 2002; Takemoto et al, 2003; Kaulin et al, 2005
3 Background Simple model of SRE channel and the scheme of its opening/closure precursor 1 (peptide-lipid micelle) precursor 2 (nonconducting cluster) small channel big channel 0.5 pа 2 sec Malev et al, 2002
4 Background Asymmetry of SRE-channel studied using PEGs addition of PEGs with different MW allows to estimate pore size Na + without PEG: penetrating PEGs reduce conductance: Cl - excluded PEGs have no effect: PEG PEG Ostroumova et al, 2007
5 Background asymmetric addition of PEGs allows to estimate pore shape cisside transside Radius value nm for cis-mouth nm for trans-mouth Ostroumova et al, 2007
6 Drug inactivation or modification: e.g. beta-lactamases Antibiotic resistance Mechanisms Alteration of target site : e.g. alteration of PBPs (penicillin binding proteins) or topoisomerases Alteration of metabolic pathways Reduced drug accumulation: increase of active efflux on the cell surface and/or decrease of drug permeability via: - Reduced expression of porins - Changed type of porin expressed - Expression of mutated porin Pic by J. Philpott, taken from The Science Creative Quarterly (
7 Porins in outer membrane of E. coli Outer Membrane Periplasmic Space Inner Membrane major porins in E. coli: OmpF, OmpC, PhoE
8 Structure of E. coli OmpF and OmpC 5 sec 0.5 ns mv 0 mv Structure of OmpC trimer (PDB code 2J1N) as viewed from the extracellular side. Latching L2 loops are colored in green, L3 loops in red, extracellular L4 loops in yellow. Three-step process of OmpC closure is observed which can be used as a test for the channel trimeric organization. OmpF and OmpC show 60% identity in amino acid sequence. Key residues are conserved in both porins but their positions are different Basle et al, 2006
9 Studies on OmpF mutants OmpF mutant G119D (L3 loop) with altered channel properties Resistance to colicin, decrease in permeation rates of sugars G119D Wild type G119D mutation divides constriction zone into two subcompartments Jeanteur et al, 1994
10 Studies on OmpF mutants R132A mutation makes bacteria more succeptible to cefepime: D113A and D121A mutations also increase the succeptibility: mean lysis diameter (mm) Bredin et al, 2002; Vidal et al, 2005
11 Studies on OmpF mutants The dark bars give the mean of the swelling rates for the five monosaccharides (glucose, galactose, mannose, fructose, and N-acetylglucosamine); the hatched bars represent the mean rate for four disaccharides (sucrose, lactose, melibiose, and maltose) Phale et al, 2001
12 Constriction zone of OmpF monomer Constriction zone at half height of the channel plays a very important role in antibiotic translocation. Different methods are used to study this process. BLM technique allows to see interactions between antibiotic and porin as time resolved fluctuations of ion current. Nestorovich et al, 2002
13 Models of translocation through the channel One-site model Solute interacts with the same binding site while translocating from left to right and vice versa P tr = translocation blocking = 2k cis trans ( k + k ) 2 on cis on k trans on on N-site model thus for perfectly symmetrical channel: k on cis =k on trans andp tr =0.5 Multiple binding sites inside the channel Kullman et al, 2002; Berezhkovskii&Bezrukov 2005; Bezrukov et al, 2007
14 Diffusion model When channel diameter is close to the size of solute molecule transport is accompanied with the entropy loss that can be compensated by intrachannel potential diffusion model : C L C R potential well in case of low concentrations: c L rl 2 >> 1; c R =0 OR C L C R potential barrier in case of high concentrations: c L rl 2 << 1; c R =0 modified from Bezrukov et al, 2007
15 Current fluctuations coincide with swelling rates modified from Yoshimura&Nikaido, 1985 and Danelon et al, 2006
16 Determination of kinetic parameters Omp36 porin from E. aerogenes homologous to E. coli OmpC cis-side = extracellular side Values of Τ cis ; k on cis ; k off cis can be obtained trans-side = intracellular side Values of Τ trans ; k on trans ; k off trans can be obtained ν, s -1 cis-side; 250 V= +50 mv 200 ν, s trans-side; V= -50 mv trans-side; V= +50 mv 150 cis-side; V= -50 mv C [ertapenem], mm trans-side; V= +50 mv trans-side; V= -50 mv C [cefepime], mm cis-side; V= +50 mv cis-side; V= -50 mv
17 Determination of kinetic parameters Values of residence time (Τ) can be used to estimate the binding model: For ertapenem: Τ cis -50mV Τ cis +50mV Τ trans -50mV Τ trans +50mV =0.142+/ ms =0.142+/ ms =0.160+/ ms =0.128+/ ms For cefepime: Τ cis -50mV Τ cis +50mV Τ trans -50mV Τ trans +50mV = / ms = / ms = / ms = / ms This shows that antibiotic molecule interacts with one binding site and we can use: P tr = translocation blocking = 2k cis trans ( k + k ) 2 on cis on k trans on on Kullman et al, 2002
18 BLM formation and single porin insertion experimental chamber oscilloscope pa pa 0 10 ms amplifier 0 10 ms 25 µm thick Teflon film Single porin insertion
19 Effect of ampicillin on E. coli OmpF and OmpC OmpF+15 mm AMP OmpC+ 15 mm AMP 1 ns 1 sec Successful blocking of OmpF and no effect with OmpC is observed Basle et al, 2006
20 OmpF mutants tested Constriction zone of OmpF E117A D113N R42A R82A negatively charged residue is substituted by uncharged positively charged residue is substituted by uncharged R132A D113N* E117Q R42A* R82A* R132A all negatively or positively charged residues are substituted by uncharged Ceccarelli et al, 2004
21 Ampicilin blocking of OmpF mutants 1.5 ns 2 sec R42A R82A R132A R42A*R82A *R132A E117A D113N Conditions: 1M KCl, ph5, 15 mm of ampicillin
22 Kinetic analysis of porin blocking v number of blocking events per second type of ν(sec -1 ) at ν(sec -1 ) at ν(c AMP =15 mm)/ OmpF C AMP =0 C AMP =15 mm ν(c AMP =0 mm) WT 0.08± ±5 520±29 R42A 0.49± ± ±0.26 E117A 0.34± ± ±0.10 R82A 0.18± ± ±0.08 R132A 0.42± ± ±0.14 Ampicillin blocks WT OmpF 100 times more effective comparing to mutants
23 MD simulations Molecular dynamic (MD) simulations provide a powerful tool to understand the mechanism at a microscopic level Possible to calculate the values of free energy landscapes during the translocation Starting point: ampicillin docked near constriction zone NH 2+ near Glu-117 CO 2- near Arg-132 D. Chandler, M. Ceccarelli
24 MD simulations Free energy landscapes for the translocation of ampicillin WT D113N energy minimum is observed near constriction zone in case of WT and D113N D113A and absent in case of D113A and R42A! R42A Angle reflects the orientation of AMP dipole along Z axis. Z cm =0 corresponds to the position of constriction zone M. Ceccarelli
25 MD simulations Unfortunately the energy minimum is also observed for R82A and R132A: M. Ceccarelli
26 Why do we see no current fluctuations? Translocation process is to fast to detect (limitations of the method) Antibiotic molecule doesn t occupy whole cross section area What measurements will give an answer?
27 Effect of enrofloxacin on OmpF and OmpC OmpC+1.5 mm Enro open state 1 blocked 2 blocked OmpF +2 mm Enro full blocking 0.2 ns 0.4 sec Conditions: 150 mm KCl, ph6, antibiotic added at cis side, V = - 50 mv
28 Future prospects Evaluation of precise interactions between porin and antibiotic molecule will help to design drugs that efficiently translocate through membrane for rapid delivery to target sites. Acknowledgements: Group of Prof. Winterhalter Group of Prof. Ceccarelli Supported by RTN-Marie Curie grant MRTN-CT Translocation Nestorovich et al, 2002
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