Cellular senescence, a major discovery of Hayflick and Moorhead (1961), is a process that generally affects cell fate and can be regarded as a hallmark of aging (Hayflick and Moorhead, 1961; López-Otn et al., 2013). Hayflick demonstrated that after a predetermined number (40-60) of population doublings, typical human diploid fibroblast cell strains cease to divide in vitro, establishing the Hayflick limit (Hayflick and Moorhead, 1961). Senescence is caused by developmental cues or various types of stress. Cells may respond to stress by causing repair, cell death, or senescence, depending on the cell type and the intensity and nature of the stress.
Senescence can occur as a result of a variety of intrinsic and extrinsic stimuli, such as progressive telomere shortening, changes in telomeric structure, mitogenic signals, oncogenic activation, radiation, oxidative and genotoxic stress, epigenetic changes, chromatin disorganization, disrupted proteostasis, mitochondrial dysfunction, inflammation, and/or tissue damage signals, irradiation or chemotherapeutic agents, nutrient deprivation.
Senescent cells have been found to accumulate exponentially with increasing chronological age in multiple tissues (Muñoz-Espín and Serrano, 2014; Hudgins et al., 2018). The early work of Hayflick and Moorhead (1961) for the first time hinted toward a relationship between senescence and aging, but subsequent discoveries have demonstrated the presence of senescent cells in vivo and an increase in their number with age supporting the hypothesis that senescence itself can drive aging and is one of its key hallmarks.
Senescent cells accumulate with age and contribute to the normal aging process as well as age-related disorders. The link between senescence, aging, and age-related pathologies, including cancer, neurodegeneration, and metabolic and cardiovascular diseases have largely fueled the senescence research field. Research in rodent models has shown that selectively eliminating senescent cells in vivo can reduce inflammation, enhance immune system function, and thereby slow the progression of age-related diseases, leading to increased health and lifespan.
For example, drugs that induce senescence, including some chemotherapeutics, are effective against cancer by suppressing their replicative potential. However, senescent cells accumulate in patients undergoing chemotherapy, presumably due to DNA damage, and are thought to contribute to unwanted side effects, particularly fatigue. Moreover, senescent cells can also contribute to cancer relapse and metastasis through the release of SASP components. Thus, the use of senolytics, which are targeted therapeutic agents against senescent cells, in chemotherapy patients may help prevent cancer relapse and alleviate some side effects. Senolytic therapies can also extend lifespan and delay age-associated physical decline in normal mice, suggesting they may be effective in treating age-related disorders. Senolytic drugs are currently being tested in humans in clinical trials for the treatment of osteoarthritis and chronic kidney disease.
However, although senescent-cell removal represents an attractive therapeutic avenue, there are many unknowns and potential pitfalls along this route. For example, our current knowledge about the rates and spatiotemporal patterns that drive the accumulation of senescent cells in both human and animal models during normal aging and in age-related diseases is limited. Another gap in knowledge relates to the degree of phenotypic heterogeneity (that is, SASP composition) between senescent cells that accumulate in vivo, not only between the acute and chronic senescent cells but also within these two classes.
Also, it will be imperative to determine the impact of senescent cell clearance on the health and lifespan of normal mice, particularly now that evidence is mounting that senescence is beneficial for tissue development and repair. Another important consideration is whether the mouse is a reliable model for recapitulating the physiological effects of senescence cell accumulation and clearance that occurs in humans.
Conversely, we should consider that, in spite of its potential beneficial effects, the removal of high percentages of senescent cells could have undesirable outcomes for human health by triggering atrophy and tissue dysfunction.
Undoubtedly, the next decade will see a tremendous expansion of data on the mechanisms, characteristics and functions of in vivo senescence, as well as the use of this information to ameliorate human age-related diseases and promote healthy lifespan.
(Co-written with Reshma Bhasker)