Poly(ADP-ribosylation) protects maternally derived histones from proteolysis after fertilization

Fertilization in sea urchins is followed by the replacement of sperm-specif ic histones by cleavage-stage histone variants recruited from maternal stor es. Such remodelling of zygote chromatin involves a cysteine proteinase tha t degrades the sperm-specific histones in a selective manner, leaving the m aternal cleavage-stage histone variants intact. The mechanism that determin es the selectivity of the sperm-histone-selective proteinase (SpH-proteinas e) was analysed by focusing on the posttranslational modification status of both sets of histones. It has previously been reported that only native cl eavage-stage histones are poly(ADP-ribosylated), whereas the sperm-specific histones are not modified. To determine whether the poly(ADP-ribose) moiet y afforded protection from degradation, the ADP-ribose polymers were remove d from the cleavage-stage histones in vitro; these proteins were then assay ed as potential substrates of the SpH-proteinase. Strikingly, the cleavage- stage histone variants were extensively degraded after the enzymic removal of their ADP-ribose moieties. In addition, the SpH cysteine proteinase was not inhibited by isolated poly(ADP-ribose) polymers. Consequently, only pol y(ADP-ribosylated) cleavage-stage histone variants are protected from prote olysis. These results demonstrate a novel role for this type of post-transl ational modification, namely the protection of nuclear proteins against nuc lear proteinases after fertilization.