2884 Current Pharmaceutical Design, 2009, 15, 2884-2892
1381-6128/09 $55.00+.00 © 2009 Bentham Science Publishers Ltd.
The Role of ABC Transporters in Protecting Cells from Bilirubin Toxicity
C. Bellarosa
1,
*
, G. Bortolussi
1
and C. Tiribelli
1,2
1
Centro Studi Fegato, AREA Science Park, Bldg Q, Campus Basovizza, ss 14 km 163.5 and
2
Department of Life
Sciences, University of Trieste, 34100 Trieste, Italy
Abstract: The ATP-Binding Cassette (ABC) superfamily is the largest transporter family known to translocate a wide va-
riety of exogenous and endogenous substrates across cell membranes. In this chapter we review the potential role of three
ABC proteins in the transport of unconjugated bilirubin (UCB). These transporters are MRP1, MRP3 and PGP (MDR1).
MRP1 is expressed at high levels in most epithelia, usually at the basolateral membrane. Among a multiplicity of sub-
strates, MRP1 mediates the ATP-dependent cellular export of UCB, and its role has been demonstrated in protecting cells
from UCB toxicity. MRP3 is an organic anion transporter whose major substrates are GSH conjugates of organic com-
pounds. Among the MRP family members, MRP3 shares the highest degree of amino acid homology with MRP1. Al-
though the hepatic expression of MRP3 has been reported to be up-regulated by bilirubin and bilirubin glucuronides, it is
unknown whether MRP3 is also involved in the transport of UCB. PGP is expressed in organs involved in the elimination
of endo- and xenobiotics and UCB is one of these substrates. Since the Km of PGP for UCB is well above pathophysi-
ological levels of Bf, it remains uncertain whether it has a role in protecting against UCB cytotoxicity.
Key Words: ATP-binding-cassette protein (ABC) protein, multidrug-resistance-associated protein 1 (MRP1), multidrug-
resistance-associated protein 3 (MRP3), P-glycoprotein (PGP), unconiugated bilirubin, bilirubin neurocytotoxicity.
BACKGROUND
The ATP-Binding Cassette (ABC) superfamily is the
largest transporter family [1] and its members have been
found in all organisms. An inventory of all 49 known and
putative human ABC transporters can be found on the Web
site of M. Muller, University of Wageningen, The Nether-
lands [2]. The designation ABC was based on the highly
conserved ATP-binding cassette, a pair of ATP-binding do-
mains, also known as nucleotide binding folds (NBF), which
are the most characteristic feature of the superfamily. ABC
transporters also contain two sets of transmembrane (TM)
domains, typically containing six membrane-spanning-
helices. The NBF contain three conserved domains: Walker
A and B domains, found in all ATP-binding proteins, and a
signature (C) motif, located just upstream of the Walker B
site. The C domain, with its consensus sequence “LeuSer-
GlyGlyGln” [3], is specific to ABC transporters and distin-
guishes them from other ATP-binding proteins [1, 4]. The
ABC proteins bind ATP and use the energy to drive the
transport of various molecules across the plasma membrane
as well as intracellular membranes of the endoplasmic reticu-
lum (ER), peroxisomes, and mitochondria. These proteins
translocate a wide variety of substrates including sugars,
amino acids, metal ions, peptides, and proteins, and a large
number of hydrophobic compounds [1]. Based on organiza-
tion of domains and amino acid homology, ABC genes can
be divided into seven families: ABCA, ABCB, ABCC, ABCD,
ABCE, ABCF and ABCG [5]. These genes are essential for
many processes in the cell. Mutations in some of the ABC
*Address correspondence to this author at the Centro Studi Fegato, Bldg Q -
AREA Science Park Basovizza, SS14 Km 163,5, 34012 Trieste, Italy; Tel:
040/375 7921; Fax: 040/375 7832; E-mail: cristina.bellarosa@csf.units.it
genes cause or contribute to many genetic disorders, includ-
ing cystic fibrosis, neurological disease specify, cholesterol
and bile acid transport defects and retinal degeneration.
Multidrug Resistance Proteins (MRPs), together with the
cystic fibrosis conductance transmembrane regulator (CFTR/
ABCC7) and the sulfonylurea receptors (SUR1/ABCC8 and
SUR2/ABCC9), comprise the 13 members of the human
ABCC family. All the C branch proteins share conserved
structural features in their nucleotide binding domains
(NBDs) that distinguish them from other ABC proteins. As
shown in Fig. (1), the MRPs can be further divided into two
subfamilies: one “long” (MRP1, -2, -3, -6, and -7) and one
“short” (MRP4, -5, -8, -9, and -10) according to the exten-
sion of the intramembrane domains [6].
Establishing the substrate specificities of the MRPs has
been, and remains, an area of considerable activity. Many
studies have focused on xenobiotic substrates because of the
potential role of the MRPs in clinical drug resistance and in
protection against a wide range of environmental toxicants.
Others have investigated the involvement of MRPs in trans-
port of endogenous substrates, including unconjugated bili-
rubin (UCB), to gain insight into possible physiological
functions of the proteins [7].
Another ABC protein involved in transport of endoge-
nous compounds is ABCB1 (MDR/PGP1) which belongs to
the ABCB subfamily. The ABCB subfamily is unique in that
it contains both four full transporters and seven half trans-
porters. ABCB1 (MDR/PGP1) was the first human ABC
transporter cloned and characterized through its ability to
confer a multidrug resistance phenotype to cancer cells [5].
The aim of this chapter is to critically review the role of
ABC proteins in the transport of unconjugated bilirubin