REVIEWS
In the assembly of a complex machine, such as a car,
every essential component must conform to carefully
defined specifications, and is therefore subject to strin-
gent quality control (QC). In the cell something similar
occurs — there are QC systems for practically every
step that leads to the synthesis of DNA, RNA and pro-
tein molecules
1–5
. As a result, the number of accumu-
lated errors in macromolecules that are ultimately
deployed by cells is extremely low.
For proteins,‘proof-reading’ occurs at the level of
transcription, translation, folding and assembly. To pass
the final QC checkpoints, a protein must typically have
reached a correctly folded conformation. This is gener-
ally the so-called ‘native’ conformation that corresponds
to the most energetically favourable state. In the case of
proteins with several subunits, proper oligomeric
assembly is usually necessary.
If the folding and maturation process fails, a protein
molecule is not transported to its final destination in
the cell, and is eventually degraded. To distinguish
between native and non-native protein conformations,
the cell uses various sensor molecules. By definition, the
sensors include the molecular chaperones, because
these interact specifically with incompletely folded pro-
teins. Molecular chaperones often have the dual role of
assisting the folding process and dispatching any improp-
erly folded proteins for destruction. The conformation-
sensing system also includes enzymes that selectively
and covalently ‘tag’ misfolded proteins for recogni-
tion by the folding and degradation machinery. The
best-known tags are ubiquitin, a small protein that is
attached to lysine side chains as a degradation signal
6
,
and glucose, which is added to the N-linked glycans of
glycoproteins as a retention signal in the endoplasmic
reticulum (ER)
7,8
.
In this review, we discuss the QC process that func-
tions on newly synthesized proteins in the ER of
eukaryotic cells. The stringent distinction between
proteins that can or cannot be transported along the
secretory pathway secures the fidelity and functional-
ity of proteins that are expressed in the extracellular
space, the plasma membrane and in the compart-
ments that are involved in secretion and endocytosis.
ER QC also regulates the degradation of those pro-
teins that are not correctly folded
9
. Disposal occurs by
a process called ER-associated degradation (ERAD);
misfolded proteins are retro-translocated from the ER
into the cytosol where they are ubiquitylated and sub-
sequently degraded by proteasomes. As ERAD has
recently been reviewed in detail in this journal
10
and
elsewhere
11,12
, we place our emphasis on aspects of
transport regulation.
Protein folding and quality control in the ER
The ER provides an environment that is optimized for
protein folding and maturation. Like the lumen of
other organelles of the secretory pathway (BOX 1), the ER
lumen is extracytosolic and is therefore topologically
equivalent to the extracellular space. Consequently, the
milieu of the ER differs from that of the cytosol with
QUALITY CONTROL IN THE
ENDOPLASMIC RETICULUM
Lars Ellgaard and Ari Helenius
The endoplasmic reticulum (ER) has a quality-control system for ‘proof-reading’ newly
synthesized proteins, so that only native conformers reach their final destinations. Non-native
conformers and incompletely assembled oligomers are retained, and, if misfolded persistently,
they are degraded. As a large fraction of ER-synthesized proteins fail to fold and mature properly,
ER quality control is important for the fidelity of cellular functions. Here, we discuss recent
progress in understanding the conformation-specific sorting of proteins at the level of ER
retention and export.
NATURE REVIEWS | MOLECULAR CELL BIOLOGY VOLUME 4 | MARCH 2003 | 181
Institute of Biochemistry,
Swiss Federal Institute of
Technology (ETH) Zürich,
Hönggerberg, CH – 8093
Zürich, Switzerland.
Correspondence to A.H.
e-mail:
ari.helenius@bc.biol.ethz.ch
doi:10.1038/nrm1052
© 2003 Nature Publishing Group