Bioorganic & Medicinal Chemistry Letters
Discovery of bisamide-heterocycles as inhibitors of scavenger
receptor BI (SR-BI)-mediated lipid uptake
a
a
c
a
Chris Dockendorff a,b, , Patrick W. Faloon , Andrew Germain , Miao Yu , Willmen Youngsaye ,
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Partha P. Nag a, Melissa Bennion a, Marsha Penman c, Thomas J. F. Nieland c, Sivaraman Dandapani a,
José R. Perez a, Benito Munoz a, Michelle A. Palmer a, Stuart L. Schreiber a,d, Monty Krieger c,
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a Center for the Science of Therapeutics, Broad Institute, 7 Cambridge Center, Cambridge, MA 02142, USA
b Department of Chemistry, Marquette University, PO Box 1881, Milwaukee, WI 53201-1881, USA
c Department of Biology, Massachusetts Institute of Technology, 77 Massachusetts Avenue, Cambridge, MA 02139, USA
d Howard Hughes Medical Institute, Broad Institute, 7 Cambridge Center, Cambridge, MA 02142, USA
a r t i c l e i n f o
a b s t r a c t
Article history:
A new series of potent inhibitors of cellular lipid uptake from HDL particles mediated by scavenger recep-
tor, class B, type I (SR-BI) was identified. The series was identified via a high-throughput screen of the
National Institutes of Health Molecular Libraries Small Molecule Repository (NIH MLSMR) that measured
the transfer of the fluorescent lipid DiI from HDL particles to CHO cells overexpressing SR-BI. The series is
characterized by a linear peptidomimetic scaffold with two adjacent amide groups, as well as an aryl-
substituted heterocycle. Analogs of the initial hit were rapidly prepared via Ugi 4-component reaction,
and select enantiopure compounds were prepared via a stepwise sequence. Structure–activity relation-
ship (SAR) studies suggest an oxygenated arene is preferred at the western end of the molecule, as well
as highly lipophilic substituents on the central and eastern nitrogens. Compound 5e, with (R)-stereo-
chemistry at the central carbon, was designated as probe ML279. Mechanistic studies indicate that
ML279 stabilizes the interaction of HDL particles with SR-BI, and its effect is reversible. It shows good
potency (IC50 = 17 nM), is non-toxic, plasma stable, and has improved solubility over our alternative
probe ML278.
Received 6 February 2015
Revised 24 March 2015
Accepted 26 March 2015
Available online 11 April 2015
Keywords:
ML279
SR-BI inhibitor
HDL receptor
Cholesterol transport
HCV
Ó 2015 The Authors. Published by Elsevier Ltd. This is an open access article under the CC BY-NC-ND license
The trafficking of lipids (e.g., cholesterol and its esters) between
tissues is critical for lipid homeostasis as well as steroidogenesis.
The key players in this transport system include lipoprotein parti-
cles (e.g., LDL and HDL) that carry the water-insoluble lipids
through the bloodstream, the enzymes that modify the lipid cargos
and/or help to transfer them from one particle to another (includ-
ing LCAT and CETP), and the receptors for the lipoprotein particles
that serve to transfer the lipids into and out of cells (i.e., uptake and
efflux). The cellular receptor for high-density lipoprotein (HDL)
particles, scavenger receptor class B, type I (SR-BI),1,2 has been
studied in detail in recent years,3–5 however a complete picture
of its mode of action is still incomplete, despite related structural
data.6 SR-BI has important effects on cardiovascular physiology,7
as well as pathogen entry (e.g., Hepatitis C virus),8–10 immune
response,11–13 and female fertility.7
We herein report our discovery of a second class of SR-BI inhi-
bitors that shows distinct advantages over those previously discov-
ered in our labs (e.g., BLT-1 and BLT-3).14 Concurrent with this
work was our discovery of the indoline–thiazole ML278,15,16 fol-
lowed soon after by the discovery of the benzo-fused lactams rep-
resented by ML312,17 described in the companion paper in this
journal.18 Several other inhibitors of SR-BI have been reported,
including HDL376,19,20 ITX-5061,21–24 R-138329, and R-154716
(Fig. 1).25 Recently, researchers at iTherX reported additional HCV
entry inhibitors, including ITX-4520, which is postulated to be an
inhibitor of SR-BI.26,27 Our discovery of the bisamide inhibitors
described herein was undertaken as part of the NIH Molecular
Libraries Program (MLP).28
To elucidate more details about the mechanism of lipid uptake
and efflux via SR-BI, and to potentially identify less toxic and more
potent small molecule probes, we undertook a high-throughput
screening (HTS) campaign measuring the uptake of the fluorescent
lipid surrogate 1,10-dioctadecyl-3,3,30,30-tetramethylindocarbocya-
nine perchlorate (DiI) from HDL particles into CHO cells overex-
pressing mouse SR-BI (ldlA[mSR-BI]).14 3046 compounds (0.96%)
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Corresponding authors. Tel.: +1 414 288 1617 (C.D.), +1 617 253 6793 (M.K.)
0960-894X/Ó 2015 The Authors. Published by Elsevier Ltd.