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Current Topics in Medicinal Chemistry, 2013, 13, 000-000 1
1568-0266/13 $58.00+.00 © 2013 Bentham Science Publishers
RND Efflux Pumps: Structural Information Translated into Function and
Inhibition Mechanisms
Paolo Ruggerone
1
, Satoshi Murakami
2
, Klaas M. Pos
3
and Attilio V. Vargiu
1,*
1
Department of Physics, University of Cagliari, S.P. 8, km 0.700, 09042 Monserrato (CA), Italy;
2
Life Science Depart-
ment, School and Graduate School of Bioscience and Biotechnology, Tokyo Institute of Technology, J2-17, 4259 Na-
gatsuta-cho, Midori-ku, Yokohama 226-8503, Japan;
3
Institute of Biochemistry, Goethe Universität Frankfurt, Max-von-
Laue-Straße 9, D-60438 Frankfurt, Germany
Abstract: Efflux pumps of the Resistance Nodulation Division (RND) superfamily play a major role in the intrinsic and
acquired resistance of Gram-negative pathogens to antibiotics. Moreover, they are largely responsible for multi-drug resis-
tance (MDR) phenomena in these bacteria. The last decade has seen a sharp increase in the number of experimental and
computational studies aimed at understanding their functional mechanisms. Most of these studies focused on the RND
drug/proton antiporter AcrB, part of the AcrAB-TolC efflux pump actively recognizing and expelling noxious agents from
the interior of bacteria. These studies have been focused on the dynamical interactions between AcrB and its substrates
and inhibitors, on the details of the proton translocation mechanisms, and on the way AcrB assembles with protein part-
ners to build up a functional pump. In this review we summarize these advances focusing on the role of AcrB.
Keywords: Multi-drug resistance, membrane barrier, efflux pumps, RND transporters, proton motive force, AcrAB-TolC, anti-
biotics, EPIs.
ANTIBIOTIC RESISTANCE AND THE MEMBRANE
BARRIER
The re-emergence of bacterial resistance to known and
new antimicrobials in the last decades is one of the major
threats to public health all over the world [1-9]. New and re-
emerging diseases are thought to be responsible for more
than 13 million deaths worldwide each year [10]. Moreover,
lethal bacterial strains, strictly confined to nosocomial set-
tings until the recent past, are found these days in the com-
munity with a severe frequency [11, 12]. This is a conse-
quence of several factors.
First, the intense (ab)use of antibiotics, biocides and her-
bicides begun in the last century has prompted the evolution
of defense strategies and the selection of resistant strains in a
wide variety of microorganisms [13-16].
Second, despite the recognized need for new antimicro-
bial agents [17, 18], pharmaceutical companies have cut their
investments in antibiotic development [17, 19-21], and only
in the last few years a new effort is ongoing in the field of
antibacterial research [22]. As a result, only a few new
classes of antibiotics have been brought to market in the last
30 years, and many companies have left the field [6, 23, 24].
Third, in addition to non-scientific concerns, the discovery
and the development of novel antibacterial agents against
multi-drug resistance has shown to be one of the most diffi-
cult challenges for the scientific community [25-28]. Tradi-
*Address correspondence to this author at the Department of Physics, Uni-
versity of Cagliari, S.P. 8, km 0.700, 09042 Monserrato (CA), Italy;
Tel: +390706754847; Fax: +390706753191;
Email: vargiu@dsf.unica.it
tional screening protocols having largely failed to address
the complexity of bacterial resistance, which requires instead
new and more powerful methods [11, 26, 29-31].
In view of these considerations, it is not surprising that
some pathogenic bacterial strains have acquired today resis-
tance to almost all known antibiotics [32-34]. These phe-
nomena, known as multi, extensive or total (or pan) drug
resistance (MDR, XDR and TDR (or PDR) respectively,
depending on how many classes of antibiotics are effective
in the treatment of the disease [35]), are related to the occur-
rence of specific resistance mechanisms such as target and
drug modification, and of more general ones which reduce
the flux of antibiotics to the bacterial cytoplasm, where their
targets reside [26, 36-38]. The reduction of intracellular drug
concentration occurs by changes in membrane permeability
(alterations and/or repression of porin expression), which
slows down the influx of most drugs [21, 26, 29, 31, 36, 38-
41]. However, this mechanism is not sufficient to explain the
high levels of resistance found in pathogenic bacteria, and
the additional contribution of active exporters, the so-called
efflux pumps, is necessary in order to achieve the character-
istic levels of intrinsic resistance [36, 37, 40, 42-54].
The interplay between influx and efflux endows bacteria
with a general mechanism of resistance that effectively keeps
the concentration of noxious agents within bacteria at suble-
thal levels. Furthermore, it gives bacteria the opportunity to
reinforce more specific mechanisms such as enzymatic inac-
tivation and modification of the drug target(s). In view of the
mechanism behind MDR, it is not surprising that this phe-
nomenon is particularly effective in Gram-negative bacteria,
where two membranes (inner and outer respectively) enve-
lope the periplasm [55-58].