Aging as a particular case of phenoptosis, the programmed death of an organism (A response to Kirkwood and Melov “On the programmed/non-programmed nature of ageing within the life history”)

The abstract of the paper published by T. B. L. Kirkwood and S. Melov in the September issue of Current Biology starts with the following categorical statement: “Compelling arguments eliminate the idea that death is generally programmed by genes for ageing” [1]. The end of the abstract is less categorical: “It is recognized that in exceptional circumstances the possibility exists for selection to favor limiting survival. In acknowledging that at least in theory, aging might occasionally be adaptive, however, the high barriers to validating actual instances of adaptive ageing are made clear” [1]. A few years ago it was hardly possible to find the latter statement in an article written by the most famous proponents of non-programmed aging. Certainly, this conclusion is accompanied by some reservations. Nevertheless, the balance between concepts of programmed and non-programmed aging seems to be really shifted to the programmed one. Such a tendency appeared in 1972 when Kerr, Willie, and Currie published their paper “Apoptosis: a basic biological phenomenon” [2]. The main message of this article was that cells of multicellular organisms are equipped with a death program. In 2002, Severin and Hyman showed that a natural signal molecule (yeast pheromone) sex-specifically kills S. cerevisiae cells [3]. I suggested that this phenomenon can be regarded as a precedent of programmed death of a unicellular organism [4]. Later it was found in our group that the mechanism of such death strikingly resembles apoptosis of higher organisms [5]. To explain the pheromone effect on yeast in terms of the traditional concept of non-programmed death of organisms, Kirkwood and Melov [1] assumed that yeast cells form in fact a multicellular organism. Such an explanation is hardly sufficient since (i) programmed death phenomena are now also described in bacteria [6-9] and (ii) an additional function of a pheromone as an inducer of the organism's death program was discovered in a mammal, the small marsupial Antechinus stuartii. Male of this rodent uses pheromone to attract females and then to kill himself after run [10]. To define all cases of programmed death of organisms, in 1997 I suggested the term "phenoptosis" [11] (for discussion, see [7, 9, 12]).