While the intrareceptor mechanisms whereby the angiotensin II type 1 (AT₁) receptor activates phospholipase C (PLC) have been extensively investigated, analogous studies of signaling through mitogen activated protein kinases (MAPK) have been lacking. We investigated MAPK activation and traditional G_q/PLC signaling in transfected cells using angiotensin II (AngII) and the signaling selective agonist Sar¹,Ile⁴,Ile⁸-AngII (SII). SII stimulated MAPK without IP₃ production and thereby stabilizes an activated receptor state linked to G-protein independent MAPK signaling. Using receptor mutagenesis, we focused on the seventh transmembrane domain and identified three key residues - Tyr²⁹², Phe²⁹³, and Thr²⁸⁷. At least three distinct activated states were revealed: (1) an AngII-stabilized state linked to G_q/PLC signaling, (2) an AngII-stabilized state connected to G-protein independent MAPK activation, and (3) a SII-stabilized state associated with G-protein independent MAPK signaling. The mutant Y292F failed to exhibit AngII-induced IP₃ turnover yet remained capable of AngII-induced MAPK activation. SII failed to stimulate MAPK in Y292F-transfected cells. Thus, Tyr²⁹² is a key epitope for activated states 1 and 3 but not required for activated state 2. While the F293L mutant retained normal AngII responses, it also showed an IP₃ response to SII, indicating that Phe²⁹³ may be involved in constraining the receptor to its inactive state. Mutations of Thr²⁸⁷ abolished all SII-induced signaling without affecting any AngII responses. Thr²⁸⁷ therefore represents a key residue for a SII-stabilized activated state. Taken together, the data identified a novel structural requirement (Thr²⁸⁷) for the SII-stabilized activated state and redefined the mechanistic roles for Tyr²⁹² and Phe²⁹³.