Abstract
Aging involves coordinated yet distinct changes in organs and systems throughout life, including changes in essential trace elements. However, how aging affects tissue element composition (ionome) and how these changes lead to dysfunction and disease remain unclear. Here, we quantified changes in the ionome across eight organs and 16 age groups of mice. This global profiling revealed novel interactions between elements at the level of tissue, age, and diet, and allowed us to achieve a broader, organismal view of the aging process. We found that while the entire ionome steadily transitions along the young‐to‐old trajectory, individual organs are characterized by distinct element changes. The ionome of mice on calorie restriction (CR) moved along a similar but shifted trajectory, pointing that at the organismal level this dietary regimen changes metabolism in order to slow down aging. However, in some tissues CR mimicked a younger state of control mice. Even though some elements changed with age differently in different tissues, in general aging was characterized by the reduced levels of elements as well as their increased variance. The dataset we prepared also allowed to develop organ‐specific, ionome‐based markers of aging that could help monitor the rate of aging. In some tissues, these markers reported the lifespan‐extending effect of CR. These aging biomarkers have the potential to become an accessible tool to test the age‐modulating effects of interventions.
Highlights
Aging is associated with systemic deleterious changes at all levels, from molecular to organismal, leading to a gradual decline in function
We explored the possibility of building organ-specific biomarkers of aging based on organ ionomes and developed a series of clocks that could track the aging process and report the effect of calorie restriction (CR). These findings offer a better understanding of aging from the perspective of element composition and provide a convenient tool that may be applied to assess the biological age of animals
We examined ionome remodeling across organs, ages, and diets, providing novel insights into the aging process and the biology of elements, and leading to the development of novel
Summary
Aging is associated with systemic deleterious changes at all levels, from molecular to organismal, leading to a gradual decline in function. The remaining five elements showed contrasting patterns in different tissues or were increased with age; for example, we observed elevated Ca in kidney and muscle, Fe in pancreas and testis, and Mo in brain and testis. The established weighted average abundances in the ionomes representing the brain, heart, liver, lung, and muscle did not correlate with age sufficiently well to have predictive power for biological age evaluation on test samples (R2 = .64, .58, .01, .50, .37, respectively). For these tissues, we were unable to discriminate between the mice on standard and CR diets.
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