Rationalizing the permeation of polar antibiotics into Gram-negative bacteria

Journal of Physics Condensed Matter

Volumn 29, Issue 11, 2017, Pages

  Scorciapino, Mariano Andrea ^a   Acosta Gutierrez, Silvia ^a   Benkerrou, Dehbia ^a   D'Agostino, Tommaso ^a   Malloci, Giuliano ^a   Samanta, Susruta ^a   Bodrenko, Igor ^a   Ceccarelli, Matteo ^a  

^a UNIVERSITY OF CAGLIARI   (Italy)

Author keywords

antibiotics; drug design; Gram negative bacteria; permeation; porins

Indexed keywords

ANTIBIOTICS; BIODEGRADATION; COMPUTER HARDWARE; CONTROLLED DRUG DELIVERY; DIAGNOSIS; MOLECULAR GRAPHICS; MOLECULAR MODELING; MOLECULES; PERMEATION; PROTEINS;

ANTIBIOTIC RESISTANCE; CONCENTRATION GRADIENTS; DRUG DESIGN; GRAM-NEGATIVE BACTERIA; MOLECULAR MODELING ALGORITHMS; PHYSICOCHEMICAL PROPERTY; PORINS; SYNERGISTIC COMBINATIONS;

BACTERIA;

ANTIINFECTIVE AGENT; PORIN;

CELL MEMBRANE PERMEABILITY; DIFFUSION; GRAM NEGATIVE BACTERIUM; MOLECULAR MODEL; PERMEABILITY;

ANTI-BACTERIAL AGENTS; CELL MEMBRANE PERMEABILITY; DIFFUSION; GRAM-NEGATIVE BACTERIA; MODELS, MOLECULAR; PERMEABILITY; PORINS;

EID: 85013219038     PISSN: 09538984     EISSN: 1361648X     Source Type: Journal    
DOI: 10.1088/1361-648X/aa543b     Document Type: Review

References (91)

1. WHO 2014 Antimicrobial Resistance: Global Report on Surveillance (Geneva: World Health Organization)
2. Silver L L 2011 Challenges of antibacterial discovery Clin. Microbiol. Rev. 24 71-109
3. Tommasi R, Brown D G, Walkup G K, Manchester J I and Miller A A 2015 ESKAPEing the labyrinth of antibacterial discovery Nat. Rev. Drug Discovery 14 529-42
4. Lewis K 2013 Platforms for antibiotic discovery Nat. Rev. Drug Discovery 12 371-87
5. The PEW Charitable Trust Antibiotics Currently in Clinical Development www.pewtrusts.org/en/multimedia/data-visualizations/2014/antibiotics-currently-in-clinical-development (Accessed: 2 January 2017)
6. Laxminarayan R et al 2013 Antibiotic resistance-the need for global solutions Lancet Infect. Dis. 13 1057-98
7. O'Neill J et al 2016 Review on Antimicrobial Resistance (London: Wellcome Trust)
8. Delcour A H 2009 Outer membrane permeability and antibiotic resistance Biochim. Biophys. Acta 1794 808-16
9. Fernandez L and Hancock R E W 2012 Adaptive and mutational resistance: role of porins and efflux pumps in drug resistance Clin. Microbiol. Rev. 25 661-81
10. Nikaido H and Vaara M 1985 Molecular basis of bacterial outer membrane permeability Microbiol. Rev. 49 1-32
11. Benz R 1988 Structure and function of porins from Gram-negative bacteria Annu. Rev. Microbiol. 42 359-93
12. Masi M and Pagès J-M 2013 Structure, function and regulation of outer membrane proteins involved in drug transport in enterobactericeae: the OmpF/C - TolC case Open Microbiol. J. 7 22-33
13. Raetz C R H and Whitfield C 2002 Lipopolysaccharide endotoxins Annu. Rev. Biochem. 71 635-700
14. Carpenter T S, Parkin J and Khalid S 2016 The free energy of small solute permeation through the Escherichia coli outer membrane has a distinctly asymmetric profile J. Phys. Chem. Lett. 7 3446-51
15. Mach T, Neves P, Spiga E, Weingart H, Winterhalter M, Ruggerone P, Ceccarelli M and Gameiro P 2008 Facilitated permeation of antibiotics across membrane channels - interaction of the quinolone moxifloxacin with the OmpF channel J. Am. Chem. Soc. 130 13301-9
16. Mahendran K R et al 2010 Molecular basis of enrofloxacin translocation through OmpF, an outer membrane channel of Escherichia coli - when binding does not imply translocation J. Phys. Chem. B 114 5170-9
17. Cama J, Bajaj H, Pagliara S, Maier T, Braun Y, Winterhalter M and Keyser U F 2015 Quantification of fluoroquinolone uptake through the outer membrane channel OmpF of Escherichia coli J. Am. Chem. Soc. 137 13836-43
18. Pagès J-M, James C E and Winterhalter M 2008 The porin and the permeating antibiotic: a selective diffusion barrier in Gram-negative bacteria Nat. Rev. Microbiol. 6 893-903
19. Kumar A, Hajjar E, Ruggerone P and Ceccarelli M 2010 Structural and dynamical properties of the porins OmpF and OmpC: insights from molecular simulations J. Phys.: Condens. Matter 22 454125
20. Kojima S and Nikaido H 2014 High salt concentrations increase permeability through OmpC channels of Escherichia coli J. Biol. Chem. 289 26464-73
21. Raj Singh P, Ceccarelli M, Lovelle M, Winterhalter M and Mahendran K R 2012 Antibiotic permeation across the OmpF channel: modulation of the affinity site in the presence of magnesium J. Phys. Chem. B 116 4433-8
22. Yoshimura F and Nikaido H 1982 Permeability of Pseudomonas aeruginosa outer membrane to hydrophilic solutes J. Bacteriol. 152 636-42
23. Hancock R E 1998 Resistance mechanisms in Pseudomonas aeruginosa and other nonfermentative Gram-negative bacteria Clin. Infect. Dis. 27 S93-9
24. Hancock R E W and Brinkman F S L 2002 Function of pseudomonas porins in uptake and efflux Annu. Rev. Microbiol. 56 17-38
25. Eren E, Vijayaraghavan J, Liu J, Cheneke B R, Touw D S, Lepore B W, Indic M, Movileanu L and van den Berg B 2012 Substrate specificity within a family of outer membrane carboxylate channels PLoS Biol. 10 e1001242
26. Tamber S, Ochs M M and Hancock R E W 2006 Role of the novel OprD family of porins in nutrient uptake in Pseudomonas aeruginosa J. Bacteriol. 188 45-54
27. Nikaido H 1994 Prevention of drug access to bacterial targets: permeability barriers and active efflux Science 264 382-8
28. Blair J M A et al 2015 AcrB drug-binding pocket substitution confers clinically relevant resistance and altered substrate specificity Proc. Natl Acad. Sci. USA 112 3511-6
29. Vaccaro L, Koronakis V and Sansom M S P 2006 Flexibility in a drug transport accessory protein: molecular dynamics simulations of MexA Biophys. J. 91 558-64
30. Sun J, Deng Z and Yan A 2014 Bacterial multidrug efflux pumps: mechanisms, physiology and pharmacological exploitations Biochem. Biophys. Res. Commun. 453 254-67
31. Cowan S, Schirmer T, Rummel G, Steiert M, Ghosh R, Pauptit R, Jansonius J and Rosenbusch J 1992 Crystal-structures explain functional-properties of 2 Escherichia coli porins Nature 358 727-33
32. Baslé A, Rummel G, Storici P, Rosenbusch J P and Schirmer T 2006 Crystal structure of osmoporin OmpC from E. coli at 2.0 Å J. Mol. Biol. 362 933-42
33. Tieleman D P and Berendsen H J 1998 A molecular dynamics study of the pores formed by Escherichia coli OmpF porin in a fully hydrated palmitoyloleoylphosphatidylcholine bilayer Biophys. J. 74 2786-801
34. Karshikoff A, Spassov V, Cowan S W, Ladenstein R and Schirmer T 1994 Electrostatic properties of two porin channels from Escherichia coli J. Mol. Biol. 240 372-84
35. Levadny V, Aguilella V M, Aguilella-Arzo M and Belaya M 2004 Interaction of a polar molecule with an ion channel Phys. Rev. E 70 041912
36. Nikaido H and Rosenberg E Y 1983 Porin channels in Escherichia coli: studies with liposomes reconstituted from purified proteins J. Bacteriol. 153 241-52
37. Pratt L A, Hsing W, Gibson K E and Silhavy T J 1996 From acids to osmZ: multiple factors influence synthesis of the OmpF and OmpC porins in Escherichia coli Mol. Microbiol. 20 911-7
38. Benz R 1994 Permeation of hydrophilic solutes through mitochondrial outer membranes: review on mitochondrial porins Biochim. Biophys. Acta 1197 167-96
39. Kojima S and Nikaido H 2013 Permeation rates of penicillins indicate that Escherichia coli porins function principally as nonspecific channels Proc. Natl Acad. Sci. 110 E2629-34
40. Mahendran K R, Kreir M, Weingart H, Fertig N and Winterhalter M 2010 Permeation of antibiotics through Escherichia coli OmpF and OmpC porins: screening for influx on a single-molecule level J. Biomol. Screen. 15 302-7
41. Ferrara L G M et al 2016 MOMP from campylobacter jejuni is a trimer of 18-stranded β-barrel monomers with a Ca2+ ion bound at the constriction zone J. Mol. Biol. 428 4528-43
42. Lou H et al 2011 Altered antibiotic transport in OmpC mutants isolated from a series of clinical strains of multi-drug resistant E. coli PLoS One 6 e25825
43. Tran Q-T, Williams S, Farid R, Erdemli G and Pearlstein R 2013 The translocation kinetics of antibiotics through porin OmpC: Insights from structure-based solvation mapping using WaterMap Proteins Struct. Funct. Bioinform. 81 291-9
44. Brown D G, May-Dracka T L, Gagnon M M and Tommasi R 2014 Trends and exceptions of physical properties on antibacterial activity for Gram-positive and Gram-negative pathogens J. Med. Chem. 57 10144-61
45. Ziervogel B K and Roux B 2013 The binding of antibiotics in OmpF porin Structure 21 76-87
46. O'Shea R and Moser H E 2008 Physicochemical properties of antibacterial compounds: implications for drug discovery J. Med. Chem. 51 2871-8
47. Kumar A, Hajjar E, Ruggerone P and Ceccarelli M 2010 Molecular simulations reveal the mechanism and the determinants for ampicillin translocation through OmpF J. Phys. Chem. B 114 9608-16
48. Danelon C, Nestorovich E M, Winterhalter M, Ceccarelli M and Bezrukov S M 2006 Interaction of zwitterionic penicillins with the OmpF channel facilitates their translocation Biophys. J. 90 1617-27
49. Hajjar E, Bessonov A, Molitor A, Kumar A, Mahendran K R, Winterhalter M, Pagès J-M, Ruggerone P and Ceccarelli M 2010 Toward screening for antibiotics with enhanced permeation properties through bacterial porins Biochemistry 49 6928-35
50. Samanta S, Scorciapino M A and Ceccarelli M 2015 Molecular basis of substrate translocation through the outer membrane channel OprD of Pseudomonas aeruginosa Phys. Chem. Chem. Phys. 17 23867-76
51. Isabella V M, Campbell A J, Manchester J, Sylvester M, Nayar A S, Ferguson K E, Tommasi R and Miller A A 2015 Toward the rational design of carbapenem uptake in Pseudomonas aeruginosa Chem. Biol. 22 535-47
52. Benz R, Schmid A and Vos-Scheperkeuter G H 1987 Mechanism of sugar transport through the sugar-specific LamB channel of Escherichia coli outer membrane J. Membr. Biol. 100 21-9
53. Schwarz G, Danelon C and Winterhalter M 2003 On translocation through a membrane channel via an internal binding site: kinetics and voltage dependence Biophys. J. 84 2990-8
54. Dutzler R, Schirmer T, Karplus M and Fischer S 2002 Translocation mechanism of long sugar chains across the maltoporin membrane channel Structure 10 1273-84
55. Nestorovich E M, Danelon C, Winterhalter M and Bezrukov S M 2002 Designed to penetrate: time-resolved interaction of single antibiotic molecules with bacterial pores Proc. Natl Acad. Sci. USA 99 9789-94
56. Nestorovich E M, Rostovtseva T K and Bezrukov S M 2003 Residue ionization and ion transport through OmpF channels Biophys. J. 85 3718-29
57. Ceccarelli M, Danelon C, Laio A and Parrinello M 2004 Microscopic mechanism of antibiotics translocation through a porin Biophys. J. 87 58-64
58. Phale P S, Philippsen A, Widmer C, Phale V P, Rosenbusch J P and Schirmer T 2001 Role of charged residues at the OmpF porin channel constriction region probed by mutagenesis and simulation Biochemistry 40 6319-25
59. Bredin J, Saint N, Malléa M, Dé E, Molle G, Pagès J-M and Simonet V 2002 Alteration of pore properties of Escherichia coli OmpF induced by mutation of key residues in anti-loop 3 region Biochem. J. 363 521-8
60. Malloci G, Vargiu A V, Serra G, Bosin A, Ruggerone P and Ceccarelli M 2015 A database of force-field parameters, dynamics, and properties of antimicrobial compounds Molecules 20 13997-4021
61. Hajjar E, Mahendran K R, Kumar A, Bessonov A, Petrescu M, Weingart H, Ruggerone P, Winterhalter M and Ceccarelli M 2010 Bridging timescales and length scales: from macroscopic flux to the molecular mechanism of antibiotic diffusion through porins Biophys. J. 98 569-75
62. Winterhalter M and Ceccarelli M 2015 Physical methods to quantify small antibiotic molecules uptake into Gram-negative bacteria Eur. J. Pharm. Biopharm. 95 63-7
63. Schmitz K S and Schurr J M 1972 Role of orientation constraints and rotational diffusion in bimolecular solution kinetics J. Phys. Chem. 76 534-45
64. Ceccarelli M, Vargiu A V and Ruggerone P 2012 A kinetic Monte Carlo approach to investigate antibiotic translocation through bacterial porins J. Phys.: Condens. Matter 24 104012
65. Berezhkovskii A M and Bezrukov S M 2005 Optimizing transport of metabolites through large channels: molecular sieves with and without binding Biophys. J. 88 L17-9
66. Bezrukov S M, Berezhkovskii A M and Szabo A 2007 Diffusion model of solute dynamics in a membrane channel: mapping onto the two-site model and optimizing the flux J. Chem. Phys. 127 115101
67. Acosta-Gutierrez S, Scorciapino M A, Bodrenko I and Ceccarelli M 2015 Filtering with electric field: the case of E. coli porins J. Phys. Chem. Lett. 6 1807-12
68. Scorciapino M A, D'Agostino T, Acosta-Gutierrez S, Malloci G, Bodrenko I and Ceccarelli M 2016 Exploiting the porin pathway for polar compound delivery into Gram-negative bacteria Future Med. Chem. 8 1047-62
69. Zahn M, D'Agostino T, Eren E, Baslé A, Ceccarelli M and van den Berg B 2015 Small-molecule transport by CarO, an abundant eight-stranded β-barrel outer membrane protein from Acinetobacter baumannii J. Mol. Biol. 427 2329-39
70. Bodrenko I, Bajaj H, Ruggerone P, Winterhalter M and Ceccarelli M 2015 Analysis of fast channel blockage: revealing substrate binding in the microsecond range Analyst 140 4820-7
71. D'Agostino T, Salis S and Ceccarelli M 2016 A kinetic model for molecular diffusion through pores Biochim. Biophys. Acta 1858 1772-7
72. Stavenger R A and Winterhalter M 2014 TRANSLOCATION project: how to get good drugs into bad bugs Sci. Transl. Med. 6 228ed7
73. Wang J, Wolf R M, Caldwell J W, Kollman P A and Case D A 2004 Development and testing of a general amber force field J. Comput. Chem. 25 1157-74
74. Doerr S, Harvey M J, Noé F and De Fabritiis G 2016 HTMD: high-throughput molecular dynamics for molecular discovery J. Chem. Theory Comput. 12 1845-52
75. Low A S, MacKenzie F M, Gould I M and Booth I R 2001 Protected environments allow parallel evolution of a bacterial pathogen in a patient subjected to long-term antibiotic therapy Mol. Microbiol. 42 619-30
76. Philippsen A, Im W, Engel A, Schirmer T, Roux B and Muller D J 2002 Imaging the electrostatic potential of transmembrane channels Biophys. J. 82 1667-76
77. Im W and Roux B 2002 Ion permeation and selectivity of OmpF porin: a theoretical study based on molecular dynamics, Brownian dynamics, and continuum electrodiffusion theory J. Mol. Biol. 322 851-69
78. Aguilella-Arzo M, Garcia-Celma J J, Cervera J, Alcaraz A and Aguilella V M 2007 Electrostatic properties and macroscopic electrodiffusion in OmpF porin and mutants Bioelectrochemistry 70 320-7
79. Gutiérrez S A, Bodrenko I, Scorciapino M A and Ceccarelli M 2016 Macroscopic electric field inside water-filled biological nanopores Phys. Chem. Chem. Phys. 18 8855-64
80. Robertson K M and Tieleman D P 2002 Orientation and interactions of dipolar molecules during transport through OmpF porin FEBS Lett. 528 53-7
81. Bajaj H, Scorciapino M A, Moynié L, Page M G P, Naismith J H, Ceccarelli M and Winterhalter M 2016 Molecular basis of filtering carbapenems by porins from β-lactam-resistant clinical strains of Escherichia coli J. Biol. Chem. 291 2837-47
82. Liu J, Eren E, Vijayaraghavan J, Cheneke B R, Indic M, van den Berg B and Movileanu L 2012 OccK Channels from Pseudomonas aeruginosa exhibit diverse single-channel electrical signatures but conserved anion selectivity Biochemistry 51 2319-30
83. Liu J, Wolfe A J, Eren E, Vijayaraghavan J, Indic M, van den Berg B and Movileanu L 2012 Cation selectivity is a conserved feature in the OccD subfamily of Pseudomonas aeruginosa Biochim. Biophys. Acta 1818 2908-16
84. Eren E, Parkin J, Adelanwa A, Cheneke B, Movileanu L, Khalid S and van den Berg B 2013 Toward understanding the outer membrane uptake of small molecules by Pseudomonas aeruginosa J. Biol. Chem. 288 12042-53
85. Pothula K R and Kleinekathöfer U 2015 Theoretical analysis of ion conductance and gating transitions in the OpdK (OccK1) channel Analyst 140 4855-64
86. Parkin J and Khalid S 2014 Atomistic molecular-dynamics simulations enable prediction of the arginine permeation pathway through OccD1/OprD from Pseudomonas aeruginosa Biophys. J. 107 1853-61
87. Nikaido H 2003 Molecular basis of bacterial outer membrane permeability revisited Microbiol. Mol. Biol. Rev. 67 593-656
88. Kullman L, Winterhalter M and Bezrukov S M 2002 Transport of maltodextrins through maltoporin: a single-channel study Biophys. J. 82 803-12
89. Laio A and Parrinello M 2002 Escaping free-energy minima Proc. Natl Acad. Sci. USA 99 12562-6
90. Torrie G M and Valleau J P 1974 Monte Carlo free energy estimates using non-Boltzmann sampling: application to the sub-critical Lennard-Jones fluid Chem. Phys. Lett. 28 578-81
91. Tiwary P and Parrinello M 2013 From metadynamics to dynamics Phys. Rev. Lett. 111 230602