A wide spectrum of CD8+ T cell responses can be elicited against antigens expressed in the liver, ranging from tolerance/unresponsive to full effector function. Identifying the factors involved could have implications for understanding and predicting the outcome of liver transplantation and viral hepatitis. Here we established a mouse model utilising recombinant adeno-associated viral vectors to investigate how CD8+ T cells respond to antigens expressed in hepatocytes.
We found that within 24 hours of antigen expression by at least 70% of hepatocytes, many naive antigen-specific CD8+ T cells were activated in the liver via direct presentation by hepatocytes. This was followed by CD8+ T cell activation in the lymph nodes and the spleen via cross presentation a day later. This suggests that primary activation of CD8+ T cells against hepatocyte-expressed antigen is compartmentalised in the first two days. These activated CD8+ T cells proliferated and developed into cytotoxic T cells in the first week. However, antigen-expressing hepatocytes were not completely cleared and the CD8+ T cells became exhausted and unresponsive over time.
In contrast, when less than 10% of hepatocytes expressed the targeted antigen, there was a more gradual activation of CD8+ T cells in the liver. Cross presentation in the lymph nodes and the spleen was also delayed. Nevertheless, these CD8+ T cells proliferated and became functional. They eliminated all antigen-expressing hepatocytes and their effector functions were maintained. Importantly, the exhaustion phenotype of the CD8+ T cells was not irreversibly imprinted during initial activation, but required continuous exposure to a high level of the intrahepatic antigen.
In summary, this study shows that intrahepatic antigen load dictates the fate of CD8+ T cell responses to liver-expressed antigens.