Pumps (almost) everywhere: Impact on resistance and pharmacokinetics
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1 Pumps (almost) everywhere: Impact on resistance and pharmacokinetics Paul M. Tulkens Unité de Pharmacologie cellulaire et moléculaire, Louvain Drug Research Institute, Université catholique de Louvain, Brussels, Belgium Groupe local d évaluation de la Médecine (GLEM) Médecine de Soins Intensifs Coordonné par les Cliniques universitaires St Luc Bruxelles Groupe local d'étude de la médecine (Soins Intensifs) 1
2 When preparing this lecture A large choice Groupe local d'étude de la médecine (Soins Intensifs) 2
3 The Menu Why active efflux or the origins of the discovery A survey of transporters in prokaryotic cells RND: the nightmare for the microbiologist From bacteria to eukaryotic cells ABC (and some of the others) bioavailability, intestine, blood-brain-barrier, kidney cancer Why we still fail Groupe local d'étude de la médecine (Soins Intensifs) 3
4 Why efflux? Efflux that saved a city slide stolen from one of the many F. Van Bambeke's presentations Groupe local d'étude de la médecine (Soins Intensifs) 4
5 An original observation with cancer cells Groupe local d'étude de la médecine (Soins Intensifs) 5
6 Most chemotherapeutic agents must reach an intracellular target enzymes nucleic acids ribosomes How can these drugs reach their target inside the cells? Groupe local d'étude de la médecine (Soins Intensifs) 6
7 Most chemotherapeutic agents must reach an intracellular target Inaba and Johnson, Cancer Res, 1977; 37: In order to survive to anticancer agents, eukaryotic cells "invented" efflux Groupe local d'étude de la médecine (Soins Intensifs) 7
8 But antibiotics were first... Who remembers that car? Groupe local d'étude de la médecine (Soins Intensifs) 8
9 Historical observations on tetracyclines Groupe local d'étude de la médecine (Soins Intensifs) 9
10 However, it took 15 years to understand In order to survive to antibiotics, bacteria "invented" efflux Groupe local d'étude de la médecine (Soins Intensifs) 10
11 Historical observations Parkinson et al. Antimicrob Agents Chemother Aug;39(8): antibiotics antifungal drugs anticancer drugs Groupe local d'étude de la médecine (Soins Intensifs) 11
12 Historical trends bacteria cancer fungi No. of publications in 10 years No. of publications in PubMed with keywords: efflux AND bacteria cancerl fungi Year (10 years interval: 0-9) Groupe local d'étude de la médecine (Soins Intensifs) 12
13 Reaching an intracellular target polar drug lipophilic drug physico-chemical properties are inadequate for reaching an intracellular target! Van Bambeke et al., Biochem. Pharmacol (2000) 60: Groupe local d'étude de la médecine (Soins Intensifs) 13
14 Reaching an intracellular target amphipathic drug most drugs are amphipathic by design, to be able to cross membrane barriers! Van Bambeke et al., Biochem. Pharmacol (2000) 60: Groupe local d'étude de la médecine (Soins Intensifs) 14
15 Intracellular chemotherapeutic agents But a diffusible compound may have potentially harmful effects! Van Bambeke et al., Biochem. Pharmacol (2000) 60: Groupe local d'étude de la médecine (Soins Intensifs) 15
16 Why efflux transporters? Extrusion by efflux pumps Van Bambeke et al., Biochem. Pharmacol (2000) 60: Groupe local d'étude de la médecine (Soins Intensifs) 16
17 Why efflux transporters? Extrusion by efflux pumps general mean of protection against cell invasion by diffusible molecules Van Bambeke et al., Biochem. Pharmacol (2000) 60: Groupe local d'étude de la médecine (Soins Intensifs) 17
18 Typical toxic diffusible substances as substrates for efflux pumps antibiotics antifungals anticancer agents Groupe local d'étude de la médecine (Soins Intensifs) 18
19 Today, there are even people believing that ALL drugs get in and out of cells by transporters Groupe local d'étude de la médecine (Soins Intensifs) 19
20 Today, there are even people believing that ALL drugs get in and out of cells by transporters Groupe local d'étude de la médecine (Soins Intensifs) 20
21 The Menu Why active efflux or the origins of the discovery A survey of transporters in prokaryotic cells RND: the nightmare for the microbiologist From bacteria to eukaryotic cells ABC (and some of the others) bioavailability, intestine, blood-brain-barrier, kidney cancer Why we still fail Groupe local d'étude de la médecine (Soins Intensifs) 21
22 Structure of efflux pumps in procaryotic cells Van Bambeke et al. JAC (2003) 51: AB pore AB porin H + AB AB AB Na + lipoprotein H + periplasm pump ATP ADP H + Na + H + RND MFS SMR MATE ABC Gram-positive RND, MFS, ABC Gram-negative Groupe local d'étude de la médecine (Soins Intensifs) 22
23 Some abbreviations ABC: ATP Binding Cassette MATE: Multi AnTimicrobial Extrusion MFS: Major Facilitator Superfamily RND: Resistance Nodulation Division SMR: Small Multidrug Resistance Groupe local d'étude de la médecine (Soins Intensifs) 23
24 Mechanisms of transport in bacteria Murakami S., Current Opinion in Structural Biology 2008, 18: Groupe local d'étude de la médecine (Soins Intensifs) 24
25 A brief survey of the many (bacterial) transporters (2003) Groupe local d'étude de la médecine (Soins Intensifs) 25
26 A brief survey of the many transporters (2003) 1. Gram Groupe local d'étude de la médecine (Soins Intensifs) 26
27 A brief survey of the many transporters (2003) 2. Gram - (part #1) Groupe local d'étude de la médecine (Soins Intensifs) 27
28 A brief survey of the many transporters (2003) 2. Gram - (part #2) Groupe local d'étude de la médecine (Soins Intensifs) 28
29 A brief survey of the many transporters (2009) 809 references Groupe local d'étude de la médecine (Soins Intensifs) 29
30 A brief survey of the many transporters: S. aureus 14 distinct transporters for S. aureus (only) in 2009 vs. 4 in Groupe local d'étude de la médecine (Soins Intensifs) 30
31 Efflux and resistance in pathogenic bacteria 1 bacteria several pumps multiresistance 1 pump several classes crossresistance of antibiotics 1 class several pumps efficacy of of antibiotics inhibitors? Groupe local d'étude de la médecine (Soins Intensifs) 31
32 The Menu Why active efflux or the origins of the discovery A survey of transporters in prokaryotic cells RND: the nightmare for the microbiologist From bacteria to eukaryotic cells ABC (and some of the others) bioavaibility, intestine, blood-brain-barrier cancer Why we still fail Groupe local d'étude de la médecine (Soins Intensifs) 32
33 General structure of an RND (AcrAB-TolC in Enterobacteriacae) Murakami S., Current Opinion in Structural Biology 2008, 18: Nikaido & Takatsuka, Biochimica et Biophysica Acta 1794 (2009) Groupe local d'étude de la médecine (Soins Intensifs) 33
34 AcrB in more details Nikaido & Takatsuka, Biochimica et Biophysica Acta 1794 (2009) Groupe local d'étude de la médecine (Soins Intensifs) 34
35 Proposed AcrB drug / H + exchange Pos K. Biochimica et Biophysica Acta 1794 (2009) Seeger et al. Curr. Drug Targets 9 (2008) Groupe local d'étude de la médecine (Soins Intensifs) 35
36 AcrAB-TolC is a multidrug transporter Pos K. Biochimica et Biophysica Acta 1794 (2009) / Seeger et al. Curr. Drug Targets 9 (2008) Groupe local d'étude de la médecine (Soins Intensifs) 36
37 AcrB has multiple entry ports Yamaguchi et al.(2015) Frontiers in Microbiology - 20 April Groupe local d'étude de la médecine (Soins Intensifs) 37
38 Interplay of RND and porins Groupe local d'étude de la médecine (Soins Intensifs) 38
39 Efflux cooperates with other mechanisms of bacterial resistance R physical clearance C O N COOH chemical clearance R R β-lactamase C O N COOH C HN O OH COOH Groupe local d'étude de la médecine (Soins Intensifs) 39
40 Efflux cooperates with other mechanisms of resistance Contributions of the AmpC β-lactamase and the AcrAB Multidrug Efflux System in Intrinsic Resistance of E. coli to β -lactams Efflux β-lactamase CMI carbenicillin CMI ofloxacin WT: intrinsic resistance! Mazzariol et al, AAC (2000) 44: Groupe local d'étude de la médecine (Soins Intensifs) 40
41 Efflux and selection of resistance to FQ Exposure to submic concentrations favors the selection of target mutations! Gyrase/ Topoisomerase Groupe local d'étude de la médecine (Soins Intensifs) 41
42 Efflux and selection of resistance Frequency of Levofloxacin-resistant mutants in Pseudomonas aeruginosa with deletions of the efflux pump operons Pump status LVX MIC Frequency of LVXresistant mutants WT mexab-oprm mexcd-oprj mexef-oprn mexab-oprm; mexef-oprn mexcd-oprj; mexef-oprn mexab-oprm; mexcd-oprj mexab-oprm; mexcd-oprj; < mexef-oprn Lomovskaya et al, AAC (1999) 43: Selection of mutants in FQ target undetectable if ALL pumps are disrupted Groupe local d'étude de la médecine (Soins Intensifs) 42
43 Increase of P. aeruginosa MICs during treatment: involvement of efflux Prevalence of MexA* and MexX* overexpressers in 62 phylogentically-related pairs of P. aeruginosa isolated from ICU patients (VAP) 9.68% DAY 0 (%) 17.74% DAY x (%) 11.29% MexA-/MexX- MexA+/MexX % 12.90% 66.13% MexX+/MexA- MexA+/MexX % 22.58% * Parts of the MexAB-OprM and MexXY-Oprm (RND pumps in P. aeruginosa) Riou et al, ECCMID 2010 Riou et al. submitted for publication Groupe local d'étude de la médecine (Soins Intensifs) 43
44 Early diagnosis could be implemented in the clinics Groupe local d'étude de la médecine (Soins Intensifs) 44
45 Early diagnosis could be implemented in the clinics Groupe local d'étude de la médecine (Soins Intensifs) 45
46 The Menu Why active efflux or the origins of the discovery A survey of transporters in prokaryotic cells RND: the nightmare for the microbiologist From bacteria to eukaryotic cells ABC (and some of the others) bioavailability, intestine, blood-brain-barrier, kidney cancer Why we still fail Groupe local d'étude de la médecine (Soins Intensifs) 46
47 Antibiotic efflux transporters are ubiquitous spectrum narrow prokaryotes distribution Gram (+) Gram (-) eukaryotes MATE SMR MFS ABC broad RND Mesaros et al., Louvain médical (2005) 124: Groupe local d'étude de la médecine (Soins Intensifs) 47
48 ABC in bacteria and eucaryotic cells Fath & Kolter, Microbiol Rev. 1993;57: Groupe local d'étude de la médecine (Soins Intensifs) 48
49 ABC in antibiotic producing organisms Transport is essential for survival of these organisms and can be intrinsically linked to resistance (it all depends how you look at it!) Groupe local d'étude de la médecine (Soins Intensifs) 49
50 ABC transporters in bacteria could also be involved in pathogenicity Groupe local d'étude de la médecine (Soins Intensifs) 50
51 ABC transporters in bacteria could be involved in pathogenicity Groupe local d'étude de la médecine (Soins Intensifs) 51
52 ABC in Fungi (with others ) Groupe local d'étude de la médecine (Soins Intensifs) 52
53 a typical ABC in Fungi (coworking with an MFS) ABC MFS Groupe local d'étude de la médecine (Soins Intensifs) 53
54 ABC transporters from bacteria to man Higgins CF, Annu. Rev. Cell Biol. 1992;8: Groupe local d'étude de la médecine (Soins Intensifs) 54
55 ABC and intracellular transport Cleves & Kelly, Curr Biol. 1996; 6: Groupe local d'étude de la médecine (Soins Intensifs) 55
56 A multiplicity of exports for protection Groupe local d'étude de la médecine (Soins Intensifs) 56
57 ABC and biliary excretion Regarding biliary excretion, we illustrate the possible contribution of the ABC transporters to the biliary excretion of xenobiotics. the multiplicities in both hepatic uptake and biliary excretion mechanisms. This helps in our understanding of the physiological adaptability of the living body in terms of the removal (detoxification) of xenobiotics Yamazaki et al. Pharm Res. 1996; 13: Groupe local d'étude de la médecine (Soins Intensifs) 57
58 Cooperation between pumps for effective extrusion of amphipathic substances from the hepatocyte (in press) Groupe local d'étude de la médecine (Soins Intensifs) 58
59 Pharmacokinetics and HIV Gulati and Gerk, J Pharm Sci. 2009; 98: Groupe local d'étude de la médecine (Soins Intensifs) 59
60 Pharmacokinetics and HIV Gulati and Gerk, J Pharm Sci. 2009; 98: Groupe local d'étude de la médecine (Soins Intensifs) 60
61 But beware! These pumps existed before the arrival of human-made drugs With regards to general immunology, an interesting suggestion is the possible involvement of the multidrug transporters in the cellular secretion of cytokines and/or chemokines. Some of these physiologically important peptides are produced without a signal sequence and recent data indicate that the expression of MDR1 is involved in the transport of these peptides through the secreting cell membranes. Also, unpublished observations link the expression of multidrug transporters to the cellmediated killing of various target cells Groupe local d'étude de la médecine (Soins Intensifs) 61
62 In eukaryotes, ABC transporters have multiple physiological functions Greenberg R International Journal for Parasitology: Drugs and Drug Resistance 4 (2014) Groupe local d'étude de la médecine (Soins Intensifs) 62
63 And they control physiological functions Sanclemente et al. J Physiol Biochem, 2009; 65: Groupe local d'étude de la médecine (Soins Intensifs) 63
64 The Menu Why active efflux or the origins of the discovery A survey of transporters in prokaryotic cells RND: the nightmare for the microbiologist From bacteria to eukaryotic cells ABC (and some of the others) bioavailability, intestine, blood-brain-barrier, kidney cancer Why we still fail Groupe local d'étude de la médecine (Soins Intensifs) 64
65 Bioavailability Oostendorp et al. Cancer Treat Rev. 2009; 35: Groupe local d'étude de la médecine (Soins Intensifs) 65
66 The family of intestinal transporters Efflux Influx Estudante et al. Advanced Drug Delivery Reviews 65 (2013) Groupe local d'étude de la médecine (Soins Intensifs) 66
67 Intestinal efflux transporters: substrates and inhibitors Estudante et al. Advanced Drug Delivery Reviews 65 (2013) Groupe local d'étude de la médecine (Soins Intensifs) 67
68 The interplay between efflux and metabolism Estudante et al. Advanced Drug Delivery Reviews 65 (2013) Groupe local d'étude de la médecine (Soins Intensifs) 68
69 Intestinal efflux and drug interactions Estudante et al. Advanced Drug Delivery Reviews 65 (2013) Groupe local d'étude de la médecine (Soins Intensifs) 69
70 Bioavailability is largely related to local transport Oostendorp et al. Cancer Treat Rev. 2009; 35: Groupe local d'étude de la médecine (Soins Intensifs) 70
71 Examples of drugs transported by one intestinal inward peptide transporter Brandsch M. Current Opinion in Pharmacology 2013, 13: Groupe local d'étude de la médecine (Soins Intensifs) 71
72 More about inward intestinal transporters Groupe local d'étude de la médecine (Soins Intensifs) 72
73 Modulation of bioavailability by excipients Groupe local d'étude de la médecine (Soins Intensifs) 73
74 Modulation of bioavailability by excipients Cremophor TM RH40, a surfactant widely used as a solubilizer in pharmaceutical preparations, inhibits both P-gp and the subfamily CYP3A in a concentration-dependent manner, which explains the increase in bioavailability of P-gp substrates in vivo Groupe local d'étude de la médecine (Soins Intensifs) 74
75 Blood-Brain Barrier multiple drug transporters BioMed Research International (2015) 2015, Article ID Groupe local d'étude de la médecine (Soins Intensifs) 75
76 Blood-Brain Barrier transporters are protective Strazielle & Ghersi-Egea (2015) Frontiers in Neuroscience 9: article Groupe local d'étude de la médecine (Soins Intensifs) 76
77 One slide on kidney or the story of tenofovir ABCC2 polymorphism has been associated with kidney damage phenotypes in patients taking tenofovir Warning: the kidney has > 26 drug transporters Moss et al. Frontiers in Pharmacology - 11 November Groupe local d'étude de la médecine (Soins Intensifs) 77
78 A global overview of transporters in eukaryotic cells Hediger et al. Molecular Aspects of Medicine 34 (2013) Groupe local d'étude de la médecine (Soins Intensifs) 78
79 The Menu Why active efflux or the origins of the discovery A survey of transporters in prokaryotic cells RND: the nightmare for the microbiologist From bacteria to eukaryotic cells ABC (and some of the others) bioavailability, intestine, blood-brain-barrier cancer and a surprise Why we still fail Groupe local d'étude de la médecine (Soins Intensifs) 79
80 Efflux-related resistance is killing patients Dean M, J Mammary Gland Biol Neoplasia. 2009; 14: Groupe local d'étude de la médecine (Soins Intensifs) 80
81 An (unanticipated?) type of resistance in plants From Dave Krupp s lectures on plants Groupe local d'étude de la médecine (Soins Intensifs) 81
82 An (unanticipated?) type of resistance in plants ATP-binding cassette (ABC) transporters and a tonoplast intrinsicprotein (TIP) may be responsible for diversion of glyphosate into the vacuole and decreasing its concentration in the chloroplasts Groupe local d'étude de la médecine (Soins Intensifs) 82
83 The Menu Why active efflux or the origins of the discovery A survey of transporters in prokaryotic cells RND: the nightmare for the microbiologist From bacteria to eukaryotic cells ABC (and some of the others) bioavaibility, intestine, blood-brain-barrier cancer and not a surprise Why we still fail Groupe local d'étude de la médecine (Soins Intensifs) 83
84 Can we really prevent efflux-mediated resistance? Groupe local d'étude de la médecine (Soins Intensifs) 84
85 Characteristics of the ideal EPI «to do» list for a winning molecule : Enhance activity of the drug under study in cells overproducing the transporter by inhibiting efflux Not affecting the drug activity in cells lacking efflux pumps Not potentiating activity or toxicity of drugs that are not effluxed Not affecting the physiological functions of the target transporter if looking for an host transporter Groupe local d'étude de la médecine (Soins Intensifs) 85
86 Examples of active but toxic molecules Against bacterial RND Against human PgP (ABC) Groupe local d'étude de la médecine (Soins Intensifs) 86
87 An example of failure Blood. 2002;100: Groupe local d'étude de la médecine (Soins Intensifs) 87
88 An example of failure Blood. 2002;100: ADE: etoposide alone ADEP: etoposide + valspodar Groupe local d'étude de la médecine (Soins Intensifs) 88
89 Potential interests of efflux pumps inhibitors for therapeutic developments? Groupe local d'étude de la médecine (Soins Intensifs) 89
90 Potential interests of efflux pumps inhibitors for therapeutic developments? Groupe local d'étude de la médecine (Soins Intensifs) 90
91 But then, wat to do? Checking, please! Moss et al. Frontiers in Pharmacology - 11 November Groupe local d'étude de la médecine (Soins Intensifs) 91
92 A still uncertain future for EPI Groupe local d'étude de la médecine (Soins Intensifs) 92
93 But still a lot of work ahead Groupe local d'étude de la médecine (Soins Intensifs) 93
94 The abundance of transporters in eukaryotic cells Hediger et al. Molecular Aspects of Medicine 34 (2013) Groupe local d'étude de la médecine (Soins Intensifs) 94
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