A cyclical, developmentally‐regulated death phenomenon in a colonial urochordate

Abstract

Botryllus schlosseri is a colonial ascidian whose asexually derived, clonally modular systems of zooids exhibit developmental synchrony. The blastogenic cycle culminates in a phase of programmed cell and zooid death called takeover, in which all functional zooids die over a 30 hr period, and are replaced by a new generation of individuals. Because of the weekly recurrence and magnitude of visceral death in this model organism, we have begun to characterize the mechanisms that govern takeover. Here we describe a monoclonal antibody (B3F12.9) that recognizes a novel 57 Kd polypeptide (under reducing conditions) localized to the perivisceral extracellular matrix (PVEM) of buds and zooids, as well as blood cells of Botryllus by immunofluorescence and immunogold labeling of tissue sections. During their active feeding phase, zooids exhibited a uniform labeling pattern of PVEM along their anteroposterior (A-P) axis. At the onset of takeover (T = 3 hr), B3F12.9 immunostaining became diffuse or absent at the anterior end, which paralleled the axis of contraction of the dying zooid, whereas the posterior end retained its labeling integrity. During mid (T = 15 hr) to late (T = 28 hr) takeover, issue damage was extensive, large blood macrophages and other B3F12.9 immunoreactive blood cells invaded the peribranchial cavity, whereas PVEM labeling gradually disappeared along the entire A-P axis. These findings indicate that takeover is a dynamic process in which extracellular matrix breakdown proceeds in a polarized fashion, beginning at the anterior end of each zooid and gradually propagating toward the posterior end. o 1992 WiIey-Liss, Inc.

Developmental cell death programs license cytotoxic cells to eliminate histocompatible partners

“…Of particular relevance, we observed significant up-regulation in genes related to autophagy, proteolysis, programmed cell death, and phagocytic clearance of cellular corpses (Dataset S1). These findings support prior observations showing intensive phagocytosis of apoptotic cells underlying colony-wide recycling between senescent zooids and developing buds during the takeover period (11,26,27).…”

“…Insight has been gained into fusion-partner resorption from observational studies showing physical similarities with the developmental period known as "takeover," or blastogenic stage D (4, 10). B. schlosseri colonies are composed of clonogenic individuals, termed "zooids," that undergo weekly cycles of death and regeneration, culminating in a massive wave of programmed cell death and removal, or takeover (11). These studies support the involvement of activated phagocytes in the elimination of tissues of the "losing" partner.…”

Botryllus schlosseri: A model ascidian for the study of asexual reproduction

“…During the shrinkage of adult zooids, the epidermis and peribranchial epithelium contract and play a special role in compressing the underlying organs: a wave of contraction moves anteroposteriorly along the body (Burighel and Schiavinato, 1984;Lauzon et al, 1992). The pharynx and peribranchial cavities collapse, the branchial walls disintegrate, and circulating phagocytes massively infiltrate senescent tissues and rapidly ingest effete cells (Burighel and Schiavinato, 1984;Cima et al, 2003).…”

“…Intermediate or mid-cycle stages, as defined by Lauzon et al (1992), correspond to stages 9/8/2 to 9/8/4 (Table 2).…”

“…Embryogenesis is rapid, and larvae for dispersal of new colonies can be obtained within a week from fertilization. In addition, it is already known as a valid model organism for studying natural apoptosis and clearance of effete cells (Burighel and Schiavinato, 1984;Lauzon et al, 1992Lauzon et al, , 1993Lauzon et al, , 2002Cima et al, 2003), allorecognition (Sabbadin, 1962(Sabbadin, , 1982Sabbadin and Astorri, 1988;Ballarin et al, 1995Ballarin et al, , 2002aRinkevich et al, 1998a;Cima et al, 2004a;De Tomaso et al, 2005;Nyholm et al, 2006), immunobiology (Ballarin et al, 1994(Ballarin et al, , 2002bBallarin and Burighel, 2006), and regeneration (Berrill, 1951;Zaniolo and Trentin, 1987;Laird et al, 2005a).…”