Immunology and Cell Biology (2004) 82, 644–650 doi:10.1111/j.1440-1711.2004.01279.x
© 2004 Australasian Society for Immunology Inc.
Special Feature
Challenges facing adjuvants for cancer immunotherapy
CIRCE MESA and LUIS E FERNÁNDEZ
Vaccine’s Department, Centre of Molecular Immunology, Havana, Cuba
Summary An adjuvant is defined as a product that increases or modulates the immune response against an antigen
(Ag). Based on this general definition many authors have postulated that the ideal adjuvant should increase the
potency of the immune response, while being non-toxic and safe. Although dozens of different adjuvants have been
shown to be effective in preclinical and clinical studies, only aluminium-based salts (Alum) and squalene–oil–water
emulsion (MF59) have been approved for human use. However, for the development of therapeutic vaccines to treat
cancer patients, the prerequisites for an ideal cancer adjuvant differ from conventional adjuvants for many reasons.
First, the patients that will receive the vaccines are immuno-compromised because of, for example, impaired
mechanisms of antigen presentation, non-responsiveness of activated T cells and enhanced inhibition of self-
reactivity by regulatory T cells. Second, the tumour Ag are usually self-derived and are, therefore, poorly
immunogenic. Third, tumours develop escape mechanisms to avoid the immune system, such as tumour editing, low
or non-expression of MHC class I molecules or secretion of suppressive cytokines. Thus, adjuvants for cancer
vaccines need to be more potent than for prophylactic vaccines and consequently may be more toxic and may even
induce autoimmune reactions. In summary, the ideal cancer adjuvant should rescue and increase the immune
response against tumours in immuno-compromised patients, with acceptable profiles of toxicity and safety. The
present review discusses the role of cancer adjuvants at the different phases of the generation of antitumour
immunity following vaccination.
Key words: immune adjuvant, impaired dendritic cell, tumour immunotherapy.
Antigen uptake and antigen-presenting cells conditioning
phase
The first phase of vaccination occurs at the site of injection
and includes not only Ag delivery into dendritic cells (DC),
but also DC activation. In many cases, a vehicle facilitates Ag
delivery and the adjuvant provides the context to promote DC
activation. For the purpose of this review the vehicle or Ag
delivery system and the adjuvant will be discussed as a single
agent that can facilitate both processes.
Dendritic cell activation
It is well known that an infectious context promotes DC
activation and the development of immunity while absence of
infection fails to do so.
1
Janeway first explained this phenom-
enon by proposing that APC possess germline-encoded
pattern recognition receptors (PRR) that recognize and are
triggered by evolutionarily conserved molecules essential to
pathogen function (the pathogen associated molecular pattern
[PAMP]), which are absent from the host cells.
2
In addition,
APC could be activated by signals made by other cells in
response to PAMP.
3
These signals are able to activate DC and
are called exogenous and endogenous ‘danger signals’, respec-
tively. These findings opened new opportunities for vaccine
design, and the concept of danger signals has been successfully
used to develop more powerful and successful adjuvants.
Among the exogenous danger signals that have demon-
strated excellent adjuvant activity are Bacillus Cal-
mette–Guerin (BCG) and bacterial non-methylated DNA
containing CpG-ODN sequences. BCG has been successfully
used as an antitumour agent in the treatment of both superfi-
cial bladder cancer and melanoma
4,5
and CpG-ODN has
shown the ability to stimulate a potent, tumour-specific
immune response in mice.
6
These preclinical investigations
have led to the ongoing development of both these agents as
components of clinical cancer immunotherapy. BCG and
CpG-ODN are known to activate DC in human and murine
systems, as indicated by induction of cytokine production,
including IL-12, and upregulation of MHC I, MHC II, CD80
and CD86
7–10
(Table 1). Another exogenous danger signal that
warns of bacterial infection is the outer membrane vesicles
derived from Neisseria meningitidis. Using this knowledge, a
new adjuvant approach in which gangliosides are incorpo-
rated into the outer membrane complex to form very small
size proteoliposomes (VSSP) has been described.
11
VSSP has
been demonstrated to have the ability to activate, in vitro and
in vivo, mouse and human DC, with corresponding IL-12p40/
p70, TNF-α and IL-6 production
12
(Table 1). This adjuvant
has the ability to render highly tolerated gangliosides immu-
nogenic.
13
Phase I trials of VSSP in melanoma and breast
cancer patients have demonstrated the safety and immuno-
genicity of these preparations.
14
Basu et al. have shown that necrotic cells, but not apop-
totic cells, can release heat shock proteins (HSP)
15
and several
research groups have shown that different HSP can activate
DC and macrophages making the HSP the first large family of
endogenous danger signals
16
(Table 1). Tumour–peptide–HSP
Correspondence: Circe Mesa, Vaccine’s Department, Centre
of Molecular Immunology, 216 esq 15, Atabey, Playa, CP 16040,
C. Habana, Cuba. Email: circe@ict.cim.sld.cu
Received 26 May 2004; accepted 6 July 2004.