ANALYSIS
NATURE METHODS | VOL.10 NO.4 | APRIL 2013 | 307
The characterization of all protein complexes of human
cells under defined physiological conditions using affinity
purification–mass spectrometry (AP-MS) is a highly desirable
step in the quest to understand the phenotypic effects of
genomic information. However, such a challenging goal has
not yet been achieved, as it requires reproducibility of the
experimental workflow and high data consistency across different
studies and laboratories. We systematically investigated the
reproducibility of a standardized AP-MS workflow by performing a
rigorous interlaboratory comparative analysis of the interactomes
of 32 human kinases. We show that it is possible to achieve high
interlaboratory reproducibility of this standardized workflow
despite differences in mass spectrometry configurations
and subtle sample preparation–related variations and that
combination of independent data sets improves the approach
sensitivity, resulting in even more-detailed networks. Our analysis
demonstrates the feasibility of obtaining a high-quality map of
the human protein interactome with a multilaboratory project.
Proteins engage in a plethora of stable and dynamic interactions
to form macromolecular assemblies, essential components of any
cellular process. The recent progress in sensitivity, throughput
and specificity of AP-MS techniques
1–8
makes this technology
ideal for the large-scale analysis of human protein complexes
9–20
.
Roughly one-tenth of the estimated 650,000 protein-protein inter-
actions (PPIs) in human cells have been experimentally observed
so far
21,22
, which suggests that the complete characterization of
the human interactome, similarly to early genome sequencing
projects, will require the collaborative effort of a larger scien-
tific community. The success of such collaborative AP-MS efforts
toward completing a reference data set for the human interaction
proteome strictly depends on the specificity and robustness in
the respective sample preparation and data acquisition methods.
Some of these issues have been addressed for collecting binary
protein-interaction information by the popular yeast two-hybrid
system
23–25
; however, no sufficient evidence has been available so
far that the protocols used to characterize complexes by AP-MS
would be robust enough to warrant the large-scale multilabora-
tory analysis necessary for the entire proteome. By analyzing the
current protein interaction databases, we found that only 25% of
annotated interactions are reproduced in an independent experi-
ment using the same human protein as a bait (Supplementary
Note 1). This rather low value could be explained by the hetero-
geneity of the experimental systems and processing pipelines.
We conducted a large-scale comparative interlaboratory study
in which 32 human protein kinases were analyzed by AP-MS in
parallel in two different laboratories: CeMM Research Center for
Molecular Medicine of the Austrian Academy of Sciences (CeMM)
and ETH Zurich (ETHZ). Samples and data were exchanged at all
steps of the procedure to measure interlaboratory reproducibility
in sample preparation, AP-MS data acquisition and computation.
Although the question of mass spectrometry data reproducibil-
ity has been addressed before
26
, to our knowledge this report is
the first study in which the interlaboratory reproducibility of the
entire AP-MS workflow, from sample preparation to bioinfor-
matic filtering, is inspected in a systematic fashion.
Our analysis showed that careful execution of a robust suite of
experimental protocols using the same biological system leads
to very high reproducibility within an individual laboratory
(98%) and high overall interlaboratory reproducibility (81%).
We found that the biochemical component affected the inter-
laboratory reproducibility slightly more than mass spectrom-
etry; however, these discrepancies were effectively minimized
by applying stringent bioinformatic filtering. The study also
showed that merging the AP-MS data sets from the two labo-
ratories improved the resolution of the protein interaction net-
work without sacrificing confidence. This work demonstrates
that large-scale analyses of the human protein interactome
by multilaboratory efforts are technically feasible and likely to
produce results that are more accurate and complete than those
of single-laboratory projects.
RESULTS
Cell-line generation, sample preparation and MS analysis
We selected 32 kinases with average basal expression levels from
kinases identified in a previous mass spectrometry survey as
Interlaboratory reproducibility of large-scale human
protein-complex analysis by standardized AP-MS
Markku Varjosalo
1,4
, Roberto Sacco
2,4
, Alexey Stukalov
2,4
, Audrey van Drogen
1
, Melanie Planyavsky
2
, Simon Hauri
1
,
Ruedi Aebersold
1,3
, Keiryn L Bennett
2
, Jacques Colinge
2
, Matthias Gstaiger
1
& Giulio Superti-Furga
2
1
Department of Biology, Institute of Molecular Systems Biology, ETH Zurich, Zurich, Switzerland.
2
CeMM Research Center for Molecular Medicine of the Austrian
Academy of Sciences, Vienna, Austria.
3
Faculty of Science, University of Zurich, Zurich, Switzerland.
4
These authors contributed equally to this work. Correspondence
should be addressed to G.S.-F. (gsuperti@cemm.oeaw.ac.at) or M.G. (gstaiger@imsb.biol.ethz.ch).
RECEIVED 27 JULY 2012; ACCEPTED 29 JANUARY 2013; PUBLISHED ONLINE 3 MARCH 2013; DOI:10.1038/NMETH.2400
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