Cell-mediated immunity was first demonstrated more
than a century ago by the Nobel Prize Laureate Ilya
Metchnikoff. By sticking a rose thorn into starfish lar-
vae, he discovered the process of phagocytosis of foreign
material and described a principle mechanism of innate
immunity. Although this observation was interpreted
for many years as a response to a foreign body, from the
current perspective it may also be considered as a host
response to injury. In 1994 Polly Matzinger proposed the
‘danger theory’, which states that the immune system can
distinguish between dangerous and innocuous endo-
genous signals
1
. It became evident that dying, stressed
or injured cells release or expose molecules on their
surface that can function as either adjuvant or danger
signals for the innate immune system
1–3
. These signals
were later called damage-associated molecular patterns
(DAMPs)
3,4
. Some DAMPs are secreted or released (such
as ATP and high mobility group protein B1 (HMGB1;
also known as amphoterin)) and others are exposed
de novo or become enriched on the outer leaflet of the
plasma membrane (such as calreticulin (CRT) and heat
shock protein 90 (HSP90)). Other DAMPs are produced
as end-stage degradation products (such as uric acid)
during the course of cell death (TABLE 1). Most of these
molecules have predominantly non-immunological
functions inside the cell before their exposure on the cell
surface or their secretion
1,3
. DAMPs that are released as a
result of cellular stress do not always trigger an immune
response: some DAMPs, such as HGMB1, can be inacti-
vated by oxidation
5
, or by caspase-dependent proteolysis,
as occurs with interleukin-33 (IL-33)
6
.
The emission of DAMPs was initially connected
with necrosis that occurred as a result of physico-
chemical injury to tissues and cells
4
. However, DAMPs
have recently been reported to be actively emitted
from dying apoptotic cells and to have a beneficial
role in anticancer therapy owing to their interaction
with the immune system
7,8
. Chemotherapy and radio-
therapy function, at least in part, by inducing apopto-
sis. As this cell death modality was widely considered
immunologically silent or even tolerogenic
9–14
, and
because the US National Cancer Institute guidelines
for drug screening for anticancer therapy require
testing with human tumours xenotransplanted into
immunocompromised mice
15
, the role of the immune
system in anticancer therapy has been systematically
neglected
16
. However, in the past few years, the con-
cept of immunogenic cell death (ICD) has emerged,
which in our opinion underlines the important role of
the immune system in the efficacy of cancer therapy
not only in mice but also in humans
17–19
. Cancer cell
lines treated ex vivo with anthracyclines, oxaliplatin,
photodynamic therapy (PDT) or γ-irradiation and then
implanted subcutaneously into syngeneic immuno-
competent mice, function as a cancer vaccine in the
absence of any adjuvants or immunostimulatory sub-
stances
4,7,8,20
. Moreover, a substantial proportion of
these mice is protected against subsequent rechallenges
with live cancer cell lines. Further research has shown
that DAMPs, such as surface exposed CRT, secreted
ATP and passively released HMGB1, and their interac-
tions with phagocytosis receptors, purinergic receptors
1
Molecular Signalling
and Cell Death Unit,
Department for Molecular
Biomedical Research, VIB,
VIB-Ghent University
Technologiepark 927, B-9052
Ghent (Zwijnaarde), Belgium.
2
Department of Biomedical
Molecular Biology,
Ghent University,
Ghent B-9052, Belgium.
3
Cell Death Research &
Therapy Unit, Department of
Cellular and Molecular
Medicine, University of
Leuven (KU Leuven), Leuven
B-3000, Belgium.
4
The Upper Airway Research
Laboratory, Department of
Oto-Rhino-Laryngology,
Ghent University Hospital,
UZ Gent, MRB, Ghent
B-9000, Belgium.
*These authors contributed
equally to this work.
Correspondence to
D.V.K. and P.V.
e-mails: Dmitri.Krysko@dmbr.
ugent.be; Peter.Vandenabeele@
dmbr.vib-ugent.be
doi:10.1038/nrc3380
Published online
15 November 2012
Immunogenic cell death and DAMPs
in cancer therapy
Dmitri V. Krysko
1,2
*, Abhishek D. Garg
3
*, Agnieszka Kaczmarek
1,2
, Olga Krysko
4
,
Patrizia Agostinis
3
*and Peter Vandenabeele
1,2
*
Abstract | Although it was thought that apoptotic cells, when rapidly phagocytosed,
underwent a silent death that did not trigger an immune response, in recent years a new
concept of immunogenic cell death (ICD) has emerged. The immunogenic characteristics of
ICD are mainly mediated by damage-associated molecular patterns (DAMPs), which include
surface-exposed calreticulin (CRT), secreted ATP and released high mobility group protein B1
(HMGB1). Most DAMPs can be recognized by pattern recognition receptors (PRRs). In this
Review, we discuss the role of endoplasmic reticulum (ER) stress and reactive oxygen
species (ROS) in regulating the immunogenicity of dying cancer cells and the effect of
therapy-resistant cancer microevolution on ICD.
REVIEWS
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