Poly(ADP-ribose) polymerase-1 (PARP-1) is a co-activator for AP-2alpha (activator protein 2alpha)-mediated transcriptional activation. In the present study, we find that the role of PARP-1 in AP-2alpha transcription is distinctly dualistic with opposing effects. Separate regions of PARP-1 interact with AP-2alpha and independently control its transcriptional activation. The C-terminus containing the catalytic domain strongly interacts with AP-2alpha, whereas low-affinity binding is seen in the middle region, which includes the breast-cancer susceptibility gene 1 C-terminal domain and automodification region. The middle region enhances AP-2alpha transcription. Even portions of this region independently interact and have partial effects on transcription. The catalytic domain strongly poly-(ADP-ribosyl)ates AP-2alpha. This modification, on the other hand, affects its DNA binding. 3-Aminobenzamide and 6(5H)-phenanthridinone that inhibit the enzymic activity significantly enhance the binding of AP-2alpha to its target sequence and increase its transcriptional activity. The enzymic activity of PARP-1 is known to be induced by stress conditions that damage cellular DNA, and the poly(ADP-ribosyl)ation of target proteins is transient in nature with a half-life of less than a minute. We hypothesize that PARP-1 enhances the transcriptional activity of AP-2alpha in normal circumstances, whereas its enzymic activity is used as a temporary shut-off mechanism during unfavourable conditions.