Genetics of Apoptosis

2.2

Apoptosis during gamete development in Hydra

Oogenesis provides a further example of apoptosis in Hydra. During oocyte
development, a large number of interstitial cells, the egg-restricted stem cells, become
committed to oogenesis. Several thousand of these interstitial cells give rise to a
macroscopically visible ‘egg patch’ on the side of the animal. One cell in the center
of the egg patch differentiates into an oocyte. The remaining cells differentiate into
nurse cells and are subsequently phagocytized by the oocyte (Honegger, 1989).
Because of their appearance, these phagocytized cells have been referred to as
Schrumpfzellen (‘shrunken cells’). After they are taken up by the oocyte, they remain
enclosed in vacuoles in the cytoplasm of the oocyte (Zihler, 1972). The nuclei become
pyknotic and chromatin is condensed at the edges of the nuclei. Moreover, the
Schrumpfzellen within the oocyte cytoplasm stain strongly with acridine orange,
suggesting that they are in a state of arrested apoptosis (Miller et al., 2000). During
cleavage, the Schrumpfzellen are distributed to blastomeres, ultimately becoming part
of the endoderm and disappearing from it only 8–10 days after hatching.
Schrumpfzellen appear to be a source of nutrition for the developing embryo, which
has to survive without food until it can catch prey for itself. How closely related nurse
cell phagocytosis is to apoptosis is not yet fully understood. The DNA fragmentation
pattern in embryos differs from that of apoptotic cells in adult Hydra. This DNA is
only partially degraded, and no laddering has been observed. DNA strand breaks were
not found by the TUNEL assay. Finally, it is still unclear whether or not caspases are
involved (Technau, personal communication).
Apoptosis also occurs during spermatogenesis in Hydra (Kuznetsov et al., 2001).
In the developing testis, interstitial cells committed to sperm-cell differentiation
accumulate in the ectoderm between epithelial cells. Spermatogonia multiply and
differentiate to form cell layers representing progressive stages of spermatogenesis in
the testis. Kuznetsov et al. have shown by acridine orange staining that sperm-cell
differentiation is accompanied by extensive cell death. Epithelial cells that form part
of the developing testis phagocytize the apoptotic corpses. Although the function of
apoptosis during Hydra spermatogenesis is not understood at the moment, it should
be noted that the same process occurs during mammalian sperm cell development,
where it is regulated by specialized Sertoli’s cells (reviewed in Print and Loveland,
2000).

2.3

Apoptosis during metamorphosis in Hydractinia

The elimination of larval structures during metamorphosis represents a classic
example of the use of apoptosis during development. Metamorphosis in the tadpole,
for instance, involves resorption of the larval tail concomitant with the building of
new adult structures. Experiments have now shown that metamorphosis in
Hydractinia is also accompanied by massive apoptosis (Seipp et al., 2001).

154 GENETICS OF APOPTOSIS