Programmed nuclear death and its relation to apoptosis and autophagy during sexual reproduction in Tetrahymena thermophila

Abstract

SUMMARY The ciliated protozoan Tetrahymena thermophila has evolved remarkable nuclear dualism that involves spatial segregation of the polyploid somatic macro- and canonical diploid germinal micronucleus in a single cytoplasm. Programmed nuclear death (PND), also referred to as nuclear apoptosis, is a remarkable catabolic process that occurs during conjugation to finish the lifespan of parental soma, in which only the parental macronucleus is eliminated from the cytoplasm, but other co-existing nuclei are unaffected. We found that PND involves unique aspects of autophagy, which differ from mammalian or yeast macroautophagy. When PND starts, the envelope of the parental macronucleus changes its nature as if it is an autophagic membrane, without the accumulation of other membranous structures from the cytoplasm. The alteration of the parental macronuclear membrane involves exposing certain sugars and phosphatidylserine on the envelope, which are members of a class of 錂eat-me 鐂 signals found on the surface of apoptotic cells, that are not found on other types of nuclei. Subsequently, small autophagic vesicles that contain mitochondria and lysosomes fuse with the nuclear envelope stepwise and release their contents into the nucleus at distinct stages. Mitochondria of Tetrahymena contain apoptosisinducing factor (AIF) and endonuclease G-like DNase, which are responsible for the nuclear condensation and kb-sized DNA fragmentation, corresponding to the early stage of the nuclear apoptosis. On the other hand, acidic lysosomal enzymes are responsible for final resorption of the nucleus. These elaborate mechanisms, unique to ciliates, ultimately achieve specific macronuclear elimination.