The serum- and glucocorticoid-inducible kinase-1 (SGK1) is a downstream effector of the phosphoinositol-3 (PI3) kinase, implicated in various cell responses including colon cancer tumorigenesis in mice. Here we investigated the role of SGK1 in the regulation of membrane androgen receptors (mAR). Using Caco2 colon tumor and embryonic kidney cells (HEK293) we report that transfections with the constitutively active SGK1 mutant (SGK1-SD) triggered mAR expression in both cell lines. Upregulated mARs were functional since their activation by testosterone albumin conjugates (TAC) induced potent apoptotic responses, downregulation of p-Akt and p-Bad expression as well as rapid actin reorganization. Moreover, SGK1-SD transfection enhanced cell motility and invasiveness, effects strongly inhibited upon mAR activation while preincubation of transfected cells with cytochalasin B, which blocks mAR-induced actin reorganization, attenuated the mAR-dependent inhibition of SGK1-stimulated migration. In line with this, the cell adhesion protein vinculin regulating actin organization was effectively de-phosphorylated in SGK1-SD-transfected cells whereas mAR activation restored vinculin phosphorylation, a finding consistent with the observed inhibition of migration upon TAC treatment in SGK1-SD-transfected cells. Finally, silencing of vinculin by appropriate siRNAs fully reversed the mAR-induced inhibition of the migratory capacity of SGK1-SD-transfected cells. The present report demonstrates for the first time that SGK1 regulates mAR expression, implying a significant role of this kinase in mAR-induced anti-tumorigenic responses.