The adaptive immune response, and in particular T cells have been shown to be important in the genesis of hypertension. In the present study, we sought to determine how angiotensin II, the NADPH oxidase and reactive oxygen species interplay with T cells to modulate their activation and ultimately hypertension. We determined that T cells express angiotensinogen, the angiotensin I-converting enzyme and renin and produce physiological levels of angiotensin II. AT₁ receptors were primarily expressed intracellularly and endogenously produced angiotensin II increased T cell activation, expression of tissue homing markers and production of the cytokine TNF. Inhibition of T cell ACE reduced TNF production; indicating endogenously produced angiotensin II has a regulatory role in this process. Studies with specific antagonists and T cells from AT₁ and AT_s mice indicated that both receptor subtypes contribute to TNF production. We found that superoxide was a critical mediator of T cell TNF production as this was significantly inhibited by PEG-SOD, but not PEG-catalase. Thus, T cells contain an endogenous renin-angiotensin system that modulates T cell function, NADPH oxidase activity and production of superoxide that in turn modulates TNF production. These findings contribute to our understanding of how angiotensin II and T cells enhance inflammation in cardiovascular disease.