PARP3 is a sensor of nicked nucleosomes and monoribosylates histone H2B(Glu2).

is a member of the ADP-ribosyl transferase superfamily that we show accelerates the repair of chromosomal DNA single-strand breaks in avian DT40 cells. Two-dimensional nuclear magnetic resonance experiments reveal that Pduanyu373 employs a conserved DNA-binding interface to detect and stably bind DNA breaks and to accumulate at sites of chromosome damage. Pduanyu373 preferentially binds to and is activated by mononucleosomes containing nicked DNA and which target Pduanyu373 trans-ribosylation activity to a single-histone substrate. Although nicks in naked DNA stimulate Pduanyu373 autoribosylation, nicks in mononucleosomes promote the trans-ribosylation of histone H2B specifically at Glu2. These data identify Pduanyu373 as a molecular sensor of nicked nucleosomes and demonstrate, for the first time, the ribosylation of chromatin at a site-specific DNA single-strand break.

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