Hormonal Regulation of Programmed Cell Death in Sea Urchin Metamorphosis

Abstract

Programmed cell death (PCD) has been identified as a key process in the metamorphic transition of indirectly developing organisms such as frogs and insects. Many marine invertebrate species with indirect development and biphasic life cycles face the challenge of completing the metamorphic transition of the larval body into a juvenile when they settle into the benthic habitat. Some key characteristics stand out during this transition in comparison to frogs and insects: (1) the transition is often remarkably fast and (2) the larval body is largely abandoned and few structures transition into the juvenile stage. In sea urchins, a group with a drastic and fast metamorphosis, development and destruction of the larval body is regulated by endocrine signals. Here we provide a brief review of the basic regulatory mechanisms of PCD in animals. We then narrow our discussion to metamorphosis with a specific emphasis on sea urchins with indirect life histories and discuss the function of thyroid hormones and histamine in larval development, metamorphosis and settlement of the sea urchin Strongylocentrotus purpuratus. We were able to annotate the large majority of PCD related genes in the sea urchin S. purpuratus and ongoing studies on sea urchin metamorphosis will shed light on the regulatory architecture underlying this dramatic life history transition. While we find overwhelming evidence for hormonal regulation of PCD in animals, especially in the context of metamorphosis, the mechanisms in many marine invertebrate groups with indirect life histories requires more work. Hence, we propose that studies of PCD in animals requires functional studies in whole organisms rather than isolated cells. We predict that future work, targeting a broader array of organisms will not only help to reveal important new functions of PCD but provide a fundamentally new perspective on its use in a diversity of taxonomic, developmental, and ecological contexts.

Thyroid hormone-dependent apoptosis during metamorphosis inCiona robustainvolves both bilaterian-ancestral and vertebrate-derived processes

“…Within the deuterostomes, the sea urchin (echinoderm) transforms from a swimming larva into a sessile juvenile (bilateral symmetric larva into radial symmetric and benthonic adult) in a few hours (Sato et al ., 2006). All eight arms of the sea urchin larva reduce from their tip to the trunk by apoptosis when treated with THs, and inhibition of apoptosis prevents the induction of metamorphosis (Saito et al ., 1998; Lutek et al ., 2018; Taylor & Heyland, 2018; Wynen & Heyland, 2021). Similar to Ciona robusta , the sea urchin has 1 RXR and 1 TR (Howard-Ashby et al ., 2006), exogenous TH treatment accelerates its metamorphosis but transcription of target genes via its TR is not activated by THs (Taylor & Heyland, 2018).…”

Comparisons of cell proliferation and cell death from tornaria larva to juvenile worm in the hemichordate Schizocardium californicum

“…The mechanism of metamorphosis in insects such as butterflies and fruit flies have also provided important comparative perspectives into the role of programmed cell death as a key event in this process [ 117 , 118 ]. Finally, cell death is implicated in the metamorphosis of marine invertebrates as they transition from planktonic larvae to benthic juveniles [ 119 ], in particular in the remodeling of the larval nervous system in gastropods [ 120 , 121 ]. In S. californicum we detected TUNEL + cells at the start of the morphological metamorphosis, most obviously around the anterior ciliary bands, which were involved in larval feeding, and fuse during metamorphosis (Fig.…”

Comparisons of cell proliferation and cell death across life histories in the hemichordate Schizocardium californicum

“…The mechanism of metamorphosis in insects such as butterflies and fruit flies have also provided important comparative perspectives into the role of programmed cell death as a key event in this process (104, 105). Finally, cell death has been implicated in the metamorphosis of marine invertebrates as they transition from planktonic larvae to benthic juveniles (106), in particular in the remodeling of the larval nervous system in gastropods (107, 108). In S. californicum we begin to detect TUNEL + cells at the start of the morphological metamorphosis, most obviously around the anterior ciliary bands, which are involved in larval feeding, but are broken down during metamorphosis (Figure 8B).…”