© 2013 Nature America, Inc. All rights reserved.
PROTOCOL
NATURE PROTOCOLS | VOL.8 NO.6 | 2013 | 1155
INTRODUCTION
Focusing on proteasome activities
The proteasome is an evolutionarily conserved proteolytic com-
plex that is responsible for the degradation of most proteins in
eukaryotic cells ranging from yeast to human. It is essential for
protein homeostasis and production of major histocompatibility
complex (MHC) class I restricted epitopes. Protein degradation is
necessary for the turnover of damaged or misfolded proteins and
regulation of biochemical pathways by lowering enzyme activity
or messenger concentration. Obviously, the proteasome is a
central protease in various cellular processes, including transcrip-
tion, translation, DNA repair, cell division and antigen presenta-
tion
1,2
. In the past decade, the proteasome became an attractive
clinical target after the approval of the proteasome inhibitor
bortezomib (Velcade) by the US Food and Drug Administration
for the treatment of multiple myeloma
3
. Encouraged by the
clinical success of bortezomib, a series of new-generation protea-
some inhibitors are being investigated as therapeutics of various
diseases; thus, both (pre)clinical and fundamental knowledge of
the activity of proteasomes is required.
The challenge of determining proteasome activity by a robust
and high-throughput method is substantial. The proteasome is
not a single protease, but a multisubunit protease cluster that,
in eukaryotes, contains active subunits with different cleavage
preferences. Mammalian 30S proteasomes contain the catalytic
20S barrel-shaped core particle (CP) capped on both sides by 19S
regulatory particles (Fig. 1). The 20S CP consists of four hepta-
meric rings assembled from α- or β-subunits (α
1–7
,β
1–7
,β
1–7
,α
1–7
)
and harbors three different peptidase activities on each β-ring
4,5
.
Crystallographic and substrate specificity studies
6
show that the
active site pockets of the β5 subunits can accommodate and cut
at the C terminus of bulky, hydrophobic amino acid residues in a
manner that resembles chymotrypsin activity. β2 subunits prefer
cleaving after basic residues and are referred to as bearing ‘trypsin-
like’ activities, whereas β1 cuts after acidic residues and is known
to have ‘caspase-like’ activity.
This constitutive 20S proteasome CP is present in all eukaryo-
tic cells. In immunocompetent tissues, three additional catalyti-
cally active β-subunits are expressed: β1i (low-molecular-weight
protein-2, LMP2), β2i (multicatalytic endopeptidase complex–
like-1, MECL1) and β5i (LMP7)
2
. The immuno-β-subunits show
comparable substrate cleavage preference, share around 50%
protein sequence identity and have different functional roles
compared with the constitutive β1, β2 and β5 subunits when
replacing them in newly assembled 20S CP, yielding the so-called
immunoproteasomes
1
. Recently, a β5t subunit was identified that
is exclusively expressed in cortical thymus epithelial cells, in which
it is incorporated in immunoproteasomes instead of β5i, yielding
the thymo-proteasome
7
. Despite this diversity, the activity of the
β-subunits is conveyed by the same mechanism of nucleophilic
attack of the N-terminal threonine (Thr1) γ-hydroxyl on the
peptide backbone
8
.
A commonly used technique to determine the proteasome activity
is by means of fluorogenic substrates. Short peptides optically
quench the aminocoumarin at their C termini, which upon cleavage
by the proteasome is released and starts to fluoresce in solution
9
.
Excellent subunit-specific fluorogenic substrates for each of the
three constitutive β-subunit activities are commercially available;
however, these substrates cannot discriminate between constitutive
and immunoproteasome activities when present in the same
cellular system. This problem is encountered during immunological
studies of antigen presentation or (pre)clinical research in immune
cells, such as leukemia and myeloma cells.
Relative quantification of proteasome activity by
activity-based protein profiling and LC-MS/MS
Nan Li, Chi-Lin Kuo, Guillem Paniagua, Hans van den Elst, Martijn Verdoes, Lianne I Willems,
Wouter A van der Linden, Mark Ruben, Eric van Genderen, Jacob Gubbens, Gilles P van Wezel,
Herman S Overkleeft & Bogdan I Florea
Gorlaeus Laboratories, Leiden Institute of Chemistry and Netherlands Proteomics Centre, Leiden, The Netherlands. Correspondence should be addressed to
B.I.F. (b.florea@chem.leidenuniv.nl)
Published online 23 May 2013; doi:10.1038/nprot.2013.065
Activity-based protein profiling (ABPP) is a functional proteomics technique for directly monitoring the expression of active
enzymes in cell extracts and living cells. The technique relies on irreversible inhibitors equipped with reactive groups (warheads)
that covalently attach to the active site of enzymes and fluorescent or affinity tags for imaging and purification purposes,
respectively. Here, a high-throughput and robust protocol for high-resolution quantitative activity-based proteasome profiling
is described. We use both panreactive and subunit-specific fluorescent activity-based probes (ABPs) to quantify the proteasome
activity in living cells, in the presence or absence of the potent proteasome inhibitor bortezomib. Active proteasome subunits
from cell lysates are affinity-purified via a biotinylated ABP. Purification from live cells involves a two-step ABP approach using
a reagent with a cell-permeable azide-warhead and postlysis installation of biotin. By means of liquid chromatography–mass
spectrometry (LC-MS)-based proteomics, we can accurately identify the enriched proteins and the active site peptides of the
enzymes, and relatively quantify all the proteasome activities in one experiment. The fluorescence ABPP protocols takes 2–3 d,
and approximately 8–10 d are needed to complete the entire protocol.