Telomere maintenance during anterior regeneration and aging in the freshwater annelid Aeolosoma viride

Abstract

Aging is a complex process involving declines in various cellular and physical functionalities, including regenerative ability. Telomere maintenance is thought to be necessary for regeneration, and telomere attrition is one mechanism that contributes to aging. However, it is unclear if aging affects regeneration owing to deterioration of telomeric maintenance. We introduce Aeolosoma viride—a freshwater annelid with strong regenerative abilities—as a new model for studying the effects of aging on telomere functions and regeneration. We show that the anterior regenerative ability of A. viride declines with age. We characterized the A. viride telomere sequence as being composed of TTAGGG repeats and identifyied the telomerase gene Avi-tert. In adult A. viride, telomerase was constantly active and telomere lengths were similar among different body sections and stably maintained with age. Notably, we found that regeneration did not result in telomere shortening at regenerating sites. Moreover, transient up-regulation of Avi-tert expression and telomerase activity was observed at regenerating sites, which might promote telomere lengthening to counteract telomere erosion resulting from cell proliferation. Our study suggests that although aging affects A. viride regeneration independent of steady-state telomere length, timely regulation of telomerase functions is critical for the regeneration process in A. viride.