Basal transcription from the human RNA polymerase III U6 promoter depends on a TATA box that recruits the TATA box-binding protein (TBP) and a proximal sequence element that recruits the small nuclear RNA (snRNA)-activating protein complex (SNAPc). TBP consists of a conserved carboxyl-terminal domain that performs all known functions of the protein and a nonconserved amino-terminal region of unknown function. Here, the amino-terminal region is shown to down-regulate binding of TBP to the U6 TATA box, mediate cooperative binding with SNAPc to the U6 promoter, and enhance U6 transcription.