ARTICLE
Auteur(s) : Carole Elbim1,
Jérôme Estaquier2,3
1Centre de Recherche des Cordeliers, Université
Pierre et Marie Curie – Paris 6, UMR S 872, Paris; Université
Paris-Descartes, UMR S 872, Paris; Inserm, U872, Paris, France
2Inserm U955, Faculté Créteil Henri-Mondor, Créteil,
France
3Assistance Publique Hôpitaux de Paris, Hôpital
Henri-Mondor, Créteil, France
accepté le 7 Novembre 2009
Polymorphonuclear neutrophils (PMN) are key components of the
first line of defense against bacterial and fungal pathogens. They
contribute to the early, innate response by rapidly migrating to
inflamed tissues, where their activation triggers microbicidal
mechanisms such as the release of proteolytic enzymes and
antimicrobial peptides, as well as the rapid production of reactive
oxygen species (ROS) in what is called the oxidative burst. ROS are
essential for bacterial killing and also potentiate inflammatory
reactions [1].
PMN are usually short-lived cells, which die spontaneously by
necrosis or apoptosis. Apoptotic PMN are recognized and
phagocytosed by macrophages, a process that is essential to resolve
inflammation [2]. In fact, this phagocytic removal of intact,
apoptotic neutrophils prevents them from releasing their cytotoxic
content into the extracellular environment, which would occur if
the cells died by necrosis [3]. The prolongation of PMN life span
is critical in their effectiveness against pathogens. Shortened PMN
survival due to apoptosis may contribute to susceptibility to
severe and recurrent infections, in some pathological situations,
through neutropenia [4, 5]; in addition, down-regulation of the
pro-inflammatory capacity of PMN has been reported during apoptosis
[6]. In contrast, inappropriate PMN survival and persistence at
sites of inflammation are thought to contribute to the pathology of
chronic inflammatory diseases [7, 8]. Thus, programmed death in PMN
needs to be well regulated in order to provide an appropriate
balance between their immune functions and their safe
clearance.
In this context, it has been shown that cytokines have a crucial
role in determining PMN cell survival. This review gives an
overview of the cell signalling involved in cytokine modulation of
PMN death.
Molecular mechanisms of neutrophil apoptosis (FIGURE 1)
Role of caspases
PMN apoptosis involves the activation of a family of cysteine
proteases, called caspases, which cleave cellular substrates at an
obligatory aspartic acid within a preferred sequence [9]. Caspase
activation is a central event in apoptosis, and results in the
proteolytic degradation of multiple substrate proteins that
contribute to the apoptotic phenotype. PMN express a variety of
regulatory and effector caspases, including caspases-1, -3 and
-8 [10, 11]. PMN contain barely detectable levels of cytochrome c;
however, the trace amount of cytochrome c present in PMN is both
necessary and sufficient for caspase activation [12]. More
recently, it has been proposed that cathepsin D, a serine protease
localized in the azurophilic granules, mediates
caspase-8 activity [13].
Role of calpains
Calpains are also cysteine proteases present in isolated PMN [14].
The level of calpastatin, a highly specific calpain inhibitor,
decreases during PMN death, leading to a drastic enhancement of the
calpain-1 activity. Activated calpain-1 cleaves, in turn,
the proapoptotic molecule Bax into an active fragment [15].
Furthermore, it has been reported that calpain mediates the
cleavage of Atg5, an autophagy-related gene required for the
formation of autophagosomes, switching autophagy to apoptosis [16].
Members of the Bcl-2 family
It is now generally agreed that PMN do not express the
anti-apoptotic protein Bcl-2, but they do express mRNA for the
anti-apoptotic proteins, Mcl-1, A1 and Bcl-xL [17, 18].
Mcl-1 and A1 proteins are expressed in PMN, and their
levels decrease prior to the onset of apoptosis [17, 18].
Mcl-1 and A1 proteins have very short half-lives
(approximately 2-3 h), whereas the half-lives of the
pro-apoptotic proteins such as Bax, Bak and Bad, are relatively
long. In the absence of de novo synthesis of Mcl-1 and A1, the
activity of the longer-lived pro-apoptotic proteins prevails and
tips the balance towards apoptosis.
Members of the TNF family
The TNFR is a transmembrane protein containing an extracellular
TNF-binding domain and a TNFR-associated death domain (TRADD) in
the cytoplasmic region of the protein [19]. PMN express two TNFRs,
TNFRSF1A (55-R, CD120a, or TNFRI) and TNFSFR1B (75-R, CD120b, or
TNFRII), and each has a slightly different role in PMN apoptosis
[20]. Gon et al. showed that TNFRI is required for
TNF-α-mediated PMN apoptosis, and its ability to promote apoptosis
is enhanced by TNFRII [21]. Blocking TNFRI, but not TNFRII, with
specific antibodies inhibits neutrophil apoptosis [21]. Additional
work using TNFR-selective mutants, has shown that TNFRI is dominant
[22]. Moreover, the ability of TNF-α to induce PMN apoptosis was
reported to be linked to ROS production. Indeed, PMN from patients
with chronic granulomatous disease, characterized by a defect in
ROS production, fail to undergo apoptosis in the presence of high
concentrations of TNF-α [20, 23].T
Table 1 Inhibition of PMN apoptosis by cytokines
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Cytokines able to inhibit PMN apoptosis
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- IL-1β, IL-2, TNF-α, IL-15, IFN-γ, IL-8, IL-18, G-CSF, GM-CSF
[28-31]
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Mechanisms
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1) Effect on anti-apoptotic molecules - Increased expression of
Mcl-1 [17, 33-35] - Increased expression of A1 [41] 2) Effect on
pro-apoptotic molecules - Decreased expression of Bax [42, 43] -
Increased phosphorylation of Bax or Bad [36, 44] leading to
decreased pro-apoptotic activity of Bax 3) Post-mitochondrial
control - Inhibition of calpain activity [48]
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Pathological situations associated with delayed PMN apoptosis and
increased levels of pro-inflammatory cytokines
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- Acute respiratory distress syndrome [50, 23] - Sepsis [51], acute
pneumonia [42] - Rheumatoid arthritis [52] - Inflammatory bowel
disease [54] - Cystic fibrosis; idiopathic fibrosis [55, 56] -
Unstable angina and acute myocardial infarction [57] - Cancer
associated with neutrophilia [42]
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Therapeutic administration of G-CSF and GM-CSF in pathological
situations associated with increased PMN apoptosis
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- Community acquired pneumonia [58] - Cancer [59] - Cyclic
neutropenia [60]
|
In vitro modulation of PMN death by cytokines
(table 1)
Among the various pro-inflammatory cytokines, it has been shown
that in vitro IL-1β, IL-2, TNF-α, IL-15, IFN-γ, G-CSF, GM-CSF and
IL-18 can prolong PMN survival [24, 25]. IL-8, a chemokine,
has also been shown to delay PMN apoptosis mediated by Fas and
TNF-α receptors [26, 27]. The reported effects of IL-6 on PMN
apoptosis are however, more controversial [28, 29]. In this
context, G-CSF and GM-CSF exert potent in vitro stimulatory effects
on PMN from HIV-infected patients at the late stage of the disease
[30, 31]. Similarly, IL-15 significantly enhanced in vitro PMN
functional activity and decreased PMN cell death in PMN from
untreated advanced HIV-infected patients [32].
Notably, TNF-α has been shown to have both pro-apoptotic and
anti-apoptotic effects toward PMN. Van de Berg et al. showed
that this bipolar effect is concentration-dependent [20]. At low
concentrations (> 0.1 ng/mL), TNF-α delays PMN apoptosis
and elicits production of proinflammatory cytokines, whereas at
higher concentrations TNF-α initiates apoptosis. Consistent with
these observations, high concentrations of TNF-α
(10-100 ng/mL) override the ability of IFN-γ and GM-CSF to
delay apoptosis [20].
Enhanced expression of the anti-apoptotic protein Mcl-1 has
been implicated in GM-CSF and IL-15-delayed PMN apoptosis [17,
33-35]. While transcriptional up-regulation of Mcl-1 is
correlated with MAPK/Erk1/2 kinase activation [36], increased
translation of Mcl-1 has been shown to depend on the PI-3K/Akt
pathway [37]. Lyn kinase, Janus kinase/signal transducer and
activator of transcription, and CD137 have also been reported
to play prominent roles in GM-CSF-mediated survival through
increased-Mcl-1 expression [38-40]. Early increases in
Mcl-1 expression may represent phosphorylation or
stabilization of Mcl-1 protein. Upregulation of the
anti-apoptotic protein A1 has also been shown to be involved
in GM-CSF-induced PMN survival [41].
Conversely, a decreased expression of the pro-apoptotic protein
Bax has been observed in aged PMN stimulated with G-CSF, GM-CSF,
IL-6 and IL-15, suggesting that the anti-apoptotic effect of
these cytokines is, in part, related to the inhibition of Bax [42,
43]. Increased phosphorylation of the pro-apoptotic molecule Bad
has been shown to be involved in PMN survival induced by GM-CSF
[36, 44]. Phosphorylation results in the binding of Bad to the
cytoplasmic 14-3-3 protein that interrupts the association
between Bad and Bcl-XL. Increased amounts of
Bcl-XL are then free to bind with Bax and prevent its
proapoptotic activity. Finally, increased Bax phosphorylation has
also been reported to regulate its activity, leading to increased
PMN survival following GM-CSF and G-CSF-treatment [45]. The
phosphorylation of Bad and Bax required PI3K/Akt activation and
appeared to be mediated by Akt itself [44-46]. Moreover, death by
neglect of PMN involves upregulation of the pro-apoptotic BH3-only
member named Bim that is counteracted by GM-CSF [47].
Finally, G-CSF has also been recently reported to inhibit PMN
apoptosis by inhibition of post-mitochondrial calpain activity
upstream of caspase-3 [48]. Interestingly, Lichtner et al.
have reported that HIV protease inhibitors reverse in vitro
apoptosis of PMN from AIDS patients by inhibiting calpain activity
[49].
In vivo PMN death and immuno-modulating effect
of cytokines (table 1)
The lifespan of PMN increases significantly once they migrate out
of the circulation and into the sites of inflammation, where they
encounter various pro-inflammatory mediators. It has been
extensively demonstrated that delayed PMN apoptosis is associated
with increased pro-inflammatory cytokine levels in several diseases
such as acute respiratory distress syndrome (ARDS) [50], sepsis
[51], rheumatoid arthritis [52], cystic fibrosis, idiopathic
fibrosis, acute pneumonia, and cancer associated with neutrophilia
[42]. In particular, dramatically elevated levels of IL-2 have
been observed in lung fluids of patients with early ARDS.
IL-2 associated with GM-CSF and G-CSF significantly
contributes to the inhibition of PMN apoptosis in bronchoalveolar
lavage fluids of patients with ARDS [53]. Increased mucosal
production of G-CSF is also related to a delay in PMN apoptosis in
inflammatory bowel disease (IBD) [54], thus providing a possible
mechanism for tissue accumulation of PMN in IBD. Enhanced PMN
survival in airways has been reported in patients with cystic
fibrosis and has been related to increased expression of G-CSF and
GM-CSF [55]. Garlichs et al. [56] reported a pronounced delay
of PMN apoptosis in patients with unstable angina and acute
myocardial infarction (ACS) associated with increased serum levels
of IFN-γ, GM-CSF, and IL-1β. Serum from ACS patients inhibits
apoptosis of PMN from healthy controls. Inflammatory cytokines
(IL-6, IL-8) during cardiopulmonary bypass prolong the functional
lifespan of PMN through modulation of apoptosis and potentiate the
inflammatory response observed after coronary bypass operation
[57]. Thus, the ability of various proinflammatory molecules to
delay PMN apoptosis is likely to be important in the initiation of
pathological inflammatory responses.
Based on these observations, hematopoietic growth factors,
especially G-CSF and GM-CSF, have been found to be effective in
various pathological situations associated with neutropenia related
to increased apoptosis. In particular, the increased PMN apoptosis
reported in patients with community-acquired pneumonia is reversed
by G-CSF treatment; prolonged PMN survival is associated with a
sustained release of anti-inflammatory cytokines [58]. Similarly,
PMN from children with cancer that have defective functional
activity and accelerated apoptosis are corrected by G-CSF and
GM-CSF in vitro [59]. Cyclic neutropenia, due to a mutation in the
gene for neutrophil elastase (ELA2), is also effectively treated
with G-CSF [60].
During the last decade, the use of non-human primate models has
allowed investigation the events involved in SIV infection in terms
of virus dynamics and immune responses [61-65]. We recently
reported that PMN from SIV-infected Rhesus macaques (RM),
chronically infected with the virulent strain SIVmac251, display
increased susceptibility to undergo apoptosis [66]. PMN apoptosis
was significantly increased in RMs progressing faster to AIDS as
compared to non-progressors RMs. PMN death was also occurring early
after infection and was prevented by inhibition of calpain
activation but not caspase activation [67]. Interestingly, levels
of inflammatory cytokines IL-8 and IL-1β that prevent in vitro
PMN death, were lower during the chronic phase in RMs progressing
towards AIDS. Thus, this decrease in inflammatory cytokines might
lead to an abnormal tendency of PMN to die. However, further
studies are necessary to evaluate the in vivo effect of
anti-apoptotic cytokines in non-human primate models as a
preclinical phase for HIV-infected individuals.
Finally, individuals with TNFR-associated periodic syndrome
(TRAPS) have a defect in the TNFR and, therefore, diminished PMN
apoptosis [68]. Patients with TRAPS experience recurrent attacks of
fever lasting > 1 week that is associated with abdominal
pain, severe arthromyalgias, rash, and periorbital edema. However,
TRAPS has not been associated with increased infections [68].
Conclusion
Because PMN are the most abundant leucocytes in the circulation,
and as they provide a primary, innate immune defense against a wide
range of microbial infections before the development of a specific
immune response, understanding the mechanisms that control their
exhaustion in the bone marrow, trafficking and survival may have
potential benefits for human diseases.
Disclosure
Funding from the ANRS to JE supported this work.
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