An electron-microscope study of cell deletion in the anuran tadpole tail during spontaneous metamorphosis with special reference to apoptosis of striated muscle fibres

TLDR

Programmed cell death (apoptosis) underlies epidermal cell loss during tadpole tail metamorphosis, a process also observed in insect larvae, though its occurrence in adult vertebrate striated muscle remains uncertain. The study aimed to investigate the cellular mechanism of tail involution in tadpoles, focusing on epidermal and striated muscle cell deletion using light and electron microscopy. Light and electron microscopy revealed that striated muscle fiber deletion occurs via a modified apoptotic pathway involving sarcoplasmic reticulum dilation, internal fragmentation, and limited surface budding due to cell size. Epidermal cells exhibit apoptotic features such as chromatin condensation, nuclear fragmentation, cytoplasmic budding, and subsequent phagocytosis by macrophage-like cells, while striated muscle fibers show similar nuclear changes and organelle preservation before macrophage-mediated degradation.

Abstract

ABSTRACT The mechanism, of cell deletion responsible for involution of the anuran tadpole tail during spontaneous metamorphosis was studied by light and electron microscopy, attention being focused on epidermis and striated muscle. The earliest indication of pending dissolution of epidermal cells was found to be aggregation of condensed chromatin beneath the nuclear envelope. This is followed by breaking up of the nucleus, and cytoplasmic condensation and budding with the production of a number of compact, membrane-bounded cell fragments with relatively well preserved organelles. These are then ingested and degraded by nearby viable cells, the majority by distinctive macrophage-like cells, which are scattered throughout the epidermis, and a few by epithelial cells. The morphological changes observed in the dying epidermal cells are the same as those described both in the ‘programmed cell death’ that plays an important role in the normal development of vertebrate embryos and in the type of cell death that has been shown to be involved in regulating the size of tissues in adult mammals under normal as well as pathological conditions; it has been suggested elsewhere that apoptosis might be a suitable name for the phenomenon. Deletion of striated muscle fibres in the tadpole tail is accomplished by a process that appears to be a modification of classical apoptosis, in which dilatation and confluence of elements of the sarcoplasmic reticulum lead to internal fragmentation, the usual surface budding presumably being precluded by the large volume and specialized structure of these cells. The early and late nuclear changes, and the apparent ultrastructural integrity of organelles in the membrane-bounded muscle fragments are typical of apoptosis, and subsequent degradation within macrophages follows the standard stereotyped pattern. An essentially similar process has been described by others in the muscles of metamorphosing insect larvae, but whether striated muscle cells in adult higher vertebrates can undergo apoptosis is still uncertain.