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Physiological Reviews, Vol. 79, No. 4, October 1999, pp. 1431-1568
Copyright ©1999 by the American Physiological Society
Department of Physiology, University of Wisconsin School of Medicine, Madison, Wisconsin
Lipton, Peter
Ischemic Cell Death in Brain Neurons. J. Neurophysiol. 79: 1431-1568, 1999. This review is directed
at understanding how neuronal death occurs in two distinct insults,
global ischemia and focal ischemia. These are the two principal rodent
models for human disease. Cell death occurs by a necrotic pathway
characterized by either ischemic/homogenizing cell change or edematous
cell change. Death also occurs via an apoptotic-like pathway that
is characterized, minimally, by DNA laddering and a dependence on
caspase activity and, optimally, by those properties, additional
characteristic protein and phospholipid changes, and morphological
attributes of apotosis. Death may also occur by autophagocytosis. The
cell death process has four major stages. The first, the induction
stage, includes several changes initiated by ischemia and reperfusion
that are very likely to play major roles in cell death. These include
inhibition (and subsequent reactivation) of electron transport,
decreased ATP, decreased pH, increased cell Ca2+, release
of glutamate, increased arachidonic acid, and also gene activation
leading to cytokine synthesis, synthesis of enzymes involved in free
radical production, and accumulation of leukocytes. These changes lead
to the activation of five damaging events, termed perpetrators. These
are the damaging actions of free radicals and their product
peroxynitrite, the actions of the Ca2+-dependent protease
calpain, the activity of phospholipases, the activity of
poly-ADPribose polymerase (PARP), and the activation of the
apoptotic pathway. The second stage of cell death involves the
long-term changes in macromolecules or key metabolites that are
caused by the perpetrators. The third stage of cell death involves
long-term damaging effects of these macromolecular and metabolite
changes, and of some of the induction processes, on critical cell
functions and structures that lead to the defined end stages of cell
damage. These targeted functions and structures include the
plasmalemma, the mitochondria, the cytoskeleton, protein synthesis, and
kinase activities. The fourth stage is the progression to the
morphological and biochemical end stages of cell death. Of these four
stages, the last two are the least well understood. Quite little is
known of how the perpetrators affect the structures and functions and
whether and how each of these changes contribute to cell death.
According to this description, the key step in ischemic cell death is
adequate activation of the perpetrators, and thus a major unifying
thread of the review is a consideration of how the changes occurring
during and after ischemia, including gene activation and synthesis of
new proteins, conspire to produce damaging levels of free radicals and
peroxynitrite, to activate calpain and other Ca2+-driven
processes that are damaging, and to initiate the apoptotic process.
Although it is not fully established for all cases, the major driving
force for the necrotic cell death process, and very possibly the other
processes, appears to be the generation of free radicals and
peroxynitrite. Effects of a large number of damaging changes can be
explained on the basis of their ability to generate free radicals in
early or late stages of damage. Several important issues are defined
for future study. These include determining the triggers for apoptosis
and autophagocytosis and establishing greater confidence in most of the
cellular changes that are hypothesized to be involved in cell death. A
very important outstanding issue is identifying the critical functional
and structural changes caused by the perpetrators of cell death. These
changes are responsible for cell death, and their identity and
mechanisms of action are almost completely unknown.
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