Development of the oocyte requires physical contact with the surrounding granulosa cells of the follicle. Contact is achieved through transzonal projections (TZPs), specialized filopodia that emanate from granulosa cells. Transforming growth factor (TGFβ) family ligands produced by the oocyte increase the number of TZPs, but how they do so is unknown. Using an inducible Cre recombinase strategy together with expression of green fluorescent protein to verify Cre activity in individual granulosa cells, we examined the effect of depleting the canonical TGFβ mediator SMAD4. We observed a 20-50% decrease in the total number of TZPs within SMAD4-depleted granulosa cell-oocyte complexes, and a 50% decrease in the number of newly generated TZPs when these granulosa cells were reaggregated with oocytes. TZPs of SMAD4-depleted cells were also longer than controls and more frequently oriented towards the oocyte and the transmembrane proteins, N-cadherin and Notch2, were reduced by 50% in these cells. SMAD4 may thus modulate a network of cell adhesion proteins that stabilize the attachment of TZPs to the oocyte, thereby amplifying signaling between the two cell types.