Effects of aging and reproduction on protein quality control in soma and gametes of Drosophila melanogaster

Abstract

SummaryIn organisms with a soma-germ demarcation, the germline must be 'preserved' such that harmful damage is not transmitted to the offspring. Keeping the progeny free of damage may be achieved by gametes enjoying elevated, and ⁄ or more functional, homeostatic maintenance systems. This possibility was approached here by testing whether the soma and maturating oocytes (eggs) dissected from female Drosophila melanogaster in reproductive ages display differential capacities for protein quality control and whether these capacities change during aging and mating. Eggs exhibited a high capacity to prevent protein aggregation, strong capacity for 26S proteasome-dependent degradation and reduced levels of oxidatively damaged (carbonylated) proteins compared to the soma. The capacity to prevent protein aggregation was not affected in either soma or eggs by age and ⁄ or mating, while the 26S proteasome capacity declined in the soma but was maintained in the eggs of aged females. However, the levels of carbonylated proteins increased with age in both soma and eggs, and this increase was more pronounced in females allowed to mate continuously. Furthermore, the levels of carbonylated proteins in the eggs of mated flies correlated negatively with the propensity of the eggs to develop into an adult fly. In young flies, mating caused a decrease in 26S proteasome capacity and an increase in protein carbonylation in the soma, but not in the eggs. These results are in line with trade-off theories of aging where aging is considered a consequence of investment in reproduction over somatic maintenance.

Parental age influences developmental stability of the progeny inDrosophila

“…In this context, it will be relevant to determine the physiological and/or genetic causes underlying the effect of parental age on offspring symmetry. We can hypothesize that the increase in FA is owing to the reduction in egg quality during ageing [31,32], a decline caused by damaged RNAs and proteins. Furthermore, instability could also result from the accumulation of DNA damage in gametes, a process that occurs both in humans [33][34][35] and flies [36].…”

The role of protein clearance mechanisms in organismal ageing and age-related diseases

“…In D. melanogaster, gonads and maturating oocytes have increased 26S proteasome activity and accumulate less damaged proteins compared with ageing somatic tissues 61,62 . Proteasome activity is already downregulated in middle-aged flies, when signs of ageing first appear 61,62 . However, maturating oocytes and gonads maintain their high proteasome activity compared with age-matched somatic tissues 61 .…”

“…Protein clearance mechanisms and stem cell maintenance Different tissues exhibit different proteasome activity 61,62 . These findings raise the intriguing question whether the proteasome is equally affected in different cell types during ageing.…”

Reproductive activity triggers accelerated male mortality and decreases lifespan: genetic and gene expression determinants in Drosophila

“…Nevertheless, alternative pathways have also been suggested to play a role in modulating reproductionlongevity relationships. For instance, evidence for tradeoffs between protein quality control in somatic tissues and eggs has recently emerged in Drosophila (Fredriksson et al, 2012). It is not farfetched to imagine that similar tradeoffs might also operate in Drosophila males, in which protein quality control could be essential for the progression of the carefully orchestrated events that occur during spermatogenesis long after most gene transcription had been shut off.…”