Current Medicinal Chemistry, 2007, 14, 1389-1397 1389
Apoptosis Remodeling in Immunosenescence: Implications for Strategies to Delay
Ageing
Massimo De Martinis
1
, Claudio Franceschi
2
, Daniela Monti
3
and Lia Ginaldi
*,1
1
Department of Internal Medicine, University of L’Aquila, Italy
2
Department of Experimental Pathology, University of Bologna, Italy
3
Department of Experimental Pathology and Oncology, University of Florence, Italy
Abstract: Immunosenescence is characterized by a peculiar remodeling of the immune system, mainly induced by lifelong
antigenic burden and oxidative stress. Apoptosis or programmed cell death plays a central role in the ageing process. Both
recurrent antigenic stimulations and oxidative metabolism by-products, impinging upon the immune system, modify the apoptotic
capability of lymphocytes, driving immunosenescence. The apoptosis remodeling, in addition to inflamm-ageing, i.e. the
upregulation of anti-stress responses and inflammatory cytokines, represents one of the major determinants of ageing rate and
longevity, as well as of the most common age-related diseases. The cells of the immune system undergo two different kinds of
apoptotic processes: activation-induced cell death (AICD), geared towards the elimination of unnecessary lymphocytes following
clonal expansion, and damage-induced cell death (DICD), particularly important for preventing the onset of neoplastic
proliferations. During senescence these apoptotic pathways are differentially modulated, with variable impacts on the ageing
process. A correct modulation of apoptosis may be useful for prolonging the lifespan or at least reducing age-related
degenerative, inflammatory and neoplastic diseases whose incidence increases with age. This review focuses on the role of
AICD and DICD dysfunction in the ageing process and highlights emerging anti-ageing therapeutical strategies offered by
apoptosis re-modulation. The challenge for the future is to identify factors and signals that regulate apoptotic processes and
determine if selective apoptosis manipulation in specific lymphocyte subsets could preserve immune function in the elderly,
contributing to successful ageing.
Keywords: Immunosenescence, apoptosis, therapeutic intervention.
INTRODUCTION controlled fashion. It plays an important role during embryonic
development, in maintaining tissue homeostasis in adults and
in responding to cellular damage, tissue injury and disease. All
cells have the intracellular machinery necessary for programmed
cell death. Whether or not they use that machinery depends on
the cell type, its tissue context, the presence or absence of
physiological death-promoting signals, and the extent to which
a cell is damaged or dysfunctional [4].
The process of ageing consists in a postmaturational
deterioration of cells and organs with the passage of time, an
increased vulnerability to challenges and a decreased ability to
survive. People are very interested in learning what they can do
to live longer as well as to remain healthy during their later
years. In view of the growing percentages of elderly people in
the population, along with an increasing incidence of age-
related diseases, such as inflammatory, degenerative and
neoplastic disorders, novel therapeutic alternatives for their
treatment are of particular interest [1,2].
On the basis of the nature of apoptosis inducing stimuli,
two main apoptotic pathways can be identified: an activation-
induced apoptosis (AICD), initiated by a variety of
physiological signals, such as the binding of ligands to their
death-promoting receptors on the cell surface, and a damage-
induced apoptosis (DICD), triggered by damage to the nucleus,
mitochondria, or other cellular components [5]. These two main
apoptotic patterns have, in reality, many links and share
common steps (mitochondria, various caspases, etc.). Major
pathways and steps in apoptotic cell death are illustrated in
(Fig. 1). During senescence, these kinds of apoptosis could be
differentially modulated, with variable impacts on the ageing
process. Changes in either of these highly complex apoptotic-
signaling networks that may occur during ageing could lead to
disease.
The immune system exhibits profound age-related changes,
collectively termed immunosenescence. The most visible of
these is the decline in protective immunity, which results from a
complex interaction of primary immune defects and
compensatory homeostatic mechanisms. The sum of these
changes is a dysregulation of many processes that normally
ensure optimal immune function.
Immunosenescence is the consequence of the continuous
attrition caused by lifelong antigenic burden and oxidative
stress. The most important characteristics of immunosenescence
(accumulation of memory and effector T cells, reduction of
naive T cells, shrinkage of T cell repertoire, reduction of the
immunological space, up-regulation of anti-stress responses
and inflammatory cytokines) are compatible with this
assumption [3].
APOPTOTIC PATHWAYS IN THE IMMUNE SYSTEM
The immune system (IS) has a unique peculiarity in respect
to other systems and organs: its physiological function is
based on multiple and successive waves of clonal expansion of
T and B lymphocytes in response to diverse and repeated
antigenic solicitations. This mechanism would rapidly lead to
saturation of the system and exhaustion of the immunological
space if each immune reaction were not down regulated with a
process of apoptosis or programmed cell death which quickly
brings the number of lymphocytes, expanded following
activation and clonal proliferation, to a level only moderately
superior to the initial one. This physiological mechanism of
activation-induced cell death is initiated, in the great majority
In this complex scenario apoptosis processes play a central
role.
APOPTOSIS
Apoptosis or programmed cell death (PCD) is a highly
orchestrated cell death process that allows cells to die in a
*Address correspondence to these authors at the Department of Internal Medicine
and Public Health, University of L’Aquila, Coppito – L’Aquila, Italy; Fax and Tel:
0039 0861 211395; E-mail: liaginaldi@alice.it
0929-8673/07 $50.00+.00 © 2007 Bentham Science Publishers Ltd.