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Aging in many animals is characterized by a failure to maintain tissue homeostasis and the loss of regenerative capacity. In this study, the ability to maintain tissue homeostasis and regenerative potential was investigated in sea urchins, a novel model to study longevity and negligible senescence. Sea urchins grow indeterminately, regenerate damaged appendages and reproduce throughout their lifespan and yet different species are reported to have very different life expectancies (ranging from 4 to more than 100 years). Quantitative analyses of cell proliferation and apoptosis indicated a low level of cell turnover in tissues of young and old sea urchins of species with different lifespans (Lytechinus variegatus, Strongylocentrotus purpuratus and Mesocentrotus franciscanus). The ability to regenerate damaged tissue was maintained with age as assessed by the regrowth of amputated spines and tube feet (motor and sensory appendages). Expression of genes involved in cell proliferation (pcna), telomere maintenance (tert) and multipotency (seawi and vasa) was maintained with age in somatic tissues. Immunolocalization of the Vasa protein to areas of the tube feet, spines, radial nerve, esophagus and a sub-population of circulating coelomocytes suggests the presence of multipotent cells that may play a role in normal tissue homeostasis and the regenerative potential of external appendages. The results indicate that regenerative potential was maintained with age regardless of lifespan, contrary to the expectation that shorter lived species would invest less in maintenance and repair.
Figure 1. Sea urchin anatomy and tissue regeneration. (A) Cross sectional view of Lytechinus variegatus showing tissues used in this study: spine, gonad, muscle from Aristotle's lantern jaw structure, esophagus, radial nerve along the inside wall of the test (shell) surrounded by the ampulla, part of the water vascular system which is continuous with the tube feet that protrude through the test. Coelomocytes freely circulate in the coelomic fluid that fills the body cavity. B through D show the spine and tube feet regeneration assay using Strongylocentrotus purpuratus. (B) Aboral view 1Â day postamputation showing tube feet and spines removed from along one of the ambulacral segments of the test from the oral to aboral surface. (C) Lateral view of the amputated region, 8Â days postamputation. (D) Lateral view of the amputated region from the same animal, 36Â days postamputation.
Figure 2. Cell proliferation and apoptosis in sea urchin tissues. Percent of cells undergoing cell proliferation (BrdU incorporation) and apoptosis (Apo ssDNA and TUNEL) in tissues of Lytechinus variegatus (A–C), Strongylocentrotus purpuratus (D–F), and Mesocentrotus franciscanus (G–I). The white bars represent small/young animals and the black bars represent large/old animals and the tissues investigated are: Aristotle's lantern muscle (ALM), esophagus (ES), radial nerve (RN), and coelomocytes (Coel). Age estimates and number of animals in each group are shown in Table 1. The data are presented as means and standard errors, and stars (*) indicate a significant difference between age groups (P < 0.05).
Figure 3. Relative gene expression for pcna, tert, seawi, and vasa in tissues of Lytechinus variegatus (Lv), Strongylocentrotus purpuratus (Sp), and Mesocentrotus franciscanus (Mf). The white bars represent small/young animals and the black bars represent large/old animals and the tissues investigated are: Aristotle's lantern muscle (Muscle), Esophagus, Radial Nerve, and Coelomocytes. Age estimates and number of animals in each group are shown in Table 1. Data are presented as means and standard errors, and stars (*) indicate a significant difference between age groups (P < 0.05).
Figure 5. Relative gene expression for pcna, tert, seawi, and vasa in tube feet from Lytechinus variegatus (Lv) and Strongylocentrotus purpuratus (Sp). The white bars represent small/young animals and the black bars represent large/old animals. Age estimates and number of animals in each group are shown in Table 1. Data are presented as means and standard errors.
Figure 6. Immunohistochemistry and immunocytochemistry of sea urchin tissues and cells using an antibody to Vasa. Esophagus, radial nerve, coelomocytes, tube foot, and spine from Lytechinus variegatus stained with DAPI or reacted with antiâ€Vasa antibody visualized with DyLightâ„¢ 488 secondary antibody. Negative control panels are tissue sections treated with only the secondary antibody. Scale bar is 100 μm.
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