Recurrent phagocytosis-induced apoptosis in the cyclical generation change of the compound ascidian Botryllus schlosseri.
Colonies of the marine, filter-feeding ascidian Botryllus schlosseri undergo cyclical generation changes or takeovers. These events are characterised by the progressive resorption of adult zooids and their replacement by their buds that grow to adult size, open their siphons and start filtering. During the take-over, tissues of adult zooids undergo extensive apoptosis; circulating, spreading phagocytes enter the effete tissues, ingest dying cells acquiring a giant size and a round morphology. Then, phagocytes re-enter the circulation where they represent a considerable fraction (more than 20%) of circulating haemocytes. In this study, we evidence that most of these circulating phagocytes show morphological and biochemical signs of apoptosis. Accordingly, these phagocytes express transcripts of orthologues of the apoptosis-related genes Bax, AIF1 and PARP1. Electron microscopy shows that giant phagocytes contain apoptotic phagocytes inside their own phagocytic vacuole. The transcript of the orthologues of the anti-apoptotic gene IAP7 was detected only in spreading phagocytes, mostly abundant in phases far from the take-over. Therefore, the presented data suggest that, at take-over, phagocytes undergo phagocytosis-induced apoptosis (PIA). In mammals, PIA is assumed to be a process assuring the killing and the complete elimination of microbes, by promoting the disposal of terminally differentiated phagocytes and the resolution of infection. In B. schlosseri, PIA assumes a so far undescribed role, being required for the control of asexual development and colony homeostasis.
Department of Biology, University of Padova, Italy.
Nicola
N
Franchi
Department of Biology, University of Padova, Italy.
Francesca
F
Ballin
Department of Biology, University of Padova, Italy. Electronic address: lucia.manni@unipd.it.
Lucia
L
Manni
Department of Biology, University of Padova, Italy.
Filippo
F
Schiavon
Department of Woman and Child Health, University of Padova, Italy.
Giuseppe
G
Basso
Department of Biology, University of Padova, Italy.
Loriano
L
Ballarin
D000818:Animals; D017209:Apoptosis; D002135:Calcium-Binding Proteins; D002478:Cells, Cultured; D004268:DNA-Binding Proteins / Q000235:genetics; D018507:Gene Expression Regulation, Developmental; D006801:Humans; D008018:Life Cycle Stages; D008840:Microfilament Proteins; D010586:Phagocytes / Q000276:immunology*; D010587:Phagocytosis; D000071137:Poly (ADP-Ribose) Polymerase-1 / Q000235:genetics / Q000378:metabolism; D014561:Urochordata / Q000502:physiology*; D051028:bcl-2-Associated X Protein / Q000235:genetics / Q000378:metabolism
C112986:AIF1 protein, human; D002135:Calcium-Binding Proteins; D004268:DNA-Binding Proteins; D008840:Microfilament Proteins; D051028:bcl-2-Associated X Protein; D000071137:Poly (ADP-Ribose) Polymerase-1
AIF1; Apoptosis-related transcripts; Bax; Botryllus; Cytofluorimetry; IAP7; PARP1; Phagocytosis-induced apoptosis; TEM; Tunicates