Study of mucosal immune responses


 

Principal Investigator : Anna George

Project Associate
John Samivel

Ph D Students
Vanitha S Raman
Shikha Gupta

Collaborators
Vineeta Bal
Satyajit Rath

The aim of the research projects of this laboratory is to analyze events in B and T cell activation and differentiation, with some emphasis on the interface between mucosal and systemic immunity. A number of related experimental approaches are being used to address the main aim. One approach, that directly addresses interactions between mucosal and systemic immunity, involves dissecting the consequences and mechanism of oral tolerance to soluble antigens of microbial and non-microbial origin. Other approaches address the role of specific ligand-receptor interactions in B cell activation and differentiation, designing ways of enhancing the immunogenecity of orally administered antigens, and analyzing signals that may contribute to the selective differentiation of B and T cells to immediate effectors versus memory cells.

Oral tolerance

In our analysis of the systemic consequences of orally encountered soluble bacterial antigens in BALB/c mice, we have reported that oral tolerance, read out as T cell hyporesponsiveness to recall antigen in vitro, could be induced with S.aureus and L.major sonicates, but not with S.typhimurium sonicate. We have now looked at the consequences of feeding-associated T cell hyporesponsiveness on antibacterial immunity and we report that in vitro T cell hyporesponsiveness does not correlate strictly with the ability of fed mice to clear a challenge infection with virulent organisms. Thus, while T cells from BALB/c mice fed with S.typhimurium sonicate did not respond better in vitro than unfed mice, they cleared a homologous challenge infection better than unfed mice did. On the other hand, mice fed with S.aureus sonicate responded far poorly than unfed mice in vitro but they were not severely compromised in their ability to clear a homologous challenge infection. These data, together with the results on cytokine KO mice reported last year, suggest that a complex and subtle relationship exists between Th1/Th2 cytokine balances and the induction and maintenance of systemic T cell hyporesponsiveness on the one hand and induction of anti-bacterial immunity on the other.

To dissect this out, we have also compared clearance of the two bacterial pathogens in four different KO mouse strains that include Th1/Th2 cytokine deficiency (IL-4, IL-10 and IFNgKOs), and TCRgd cell deficiency (TCRd KO). We find that oral administration of the two sonicates has quite distinct effects on bacterial clearance. At appropriate challenge doses, fed wild-type C57BL/6 mice do not clear S.aureus challenge as well as unfed controls do and this pattern is seen in the all four KO strains. On the other hand, fed wild-type C57BL/6 mice clear S.typhimurium challenge better than unfed mice and this pattern is seen in IL-4, IL-10 and TCRd-KO mice but not in IFNg KO mice.

S.aureu is an extracellular, non-enteric pathogen that is effectively cleared by antibodies generated with the help of Th2 cytokines and S.typhimurium is an intracellular, enteric pathogen that is cleared by a combination of antibodies, activated macrophages and cytotoxic T cells, with contributions from Th1 and Th2 cytokines. We have now initiated experiments to look at the clearance of L.major, an intracellular non-enteric pathogen that requires a Th1-dominated response for parasite clearance in these KO mouse strains. L.major sonicate behaves like S.aureus sonicate in inducing oral tolerance as read out by T cell recall responses in vitro, and these experiments should be useful in helping us dissect out the interplay between oral feeding and cytokine balances in systemic anti-microbial immunity.

B and T cell activation and differentiation

Over the current reporting year, we have analyzed the effect of CD27 ligation on B cell responses in vivo. We report that primary antibody responses are poorer in mice immunized with a T-dependent antigen in the presence of anti-CD27 than in control mice. Thus, ligation of CD27 in vivo during B cell priming inhibits plasma cell generation, as seen with in the in vitro B cell activation systems reported last year. Since plasma cell generation and memory cell generation are mutually exclusive consequences of B cell activation, these data raise the possibility that the reduced terminal differentiation that occurs in the presence of anti-CD27 may be accompanied by an enhanced memory cell pool. We have initiated experiments to test this possibility.

We have also been analysing the effect of ICAM-1 deficiency on B and T cell maturation and priming. We report that in ICAM-1 KO mice, B cell maturation is normal as assessed by proportions of mature and immature B cells in the periphery. However, they have relatively more B cells in the spleen than wild-type mice, suggesting that export and/or survival of the cells may differ. Polyclonal responses to LPS and immunoglobulin cross-linking are similar when normalized for B cell numbers, but preliminary experiments indicate that they may respond less well to surface IgM crosslinking. We have also found that while T cells in the KO mice do get primed following immunization, recall responses decay faster than in wild-type mice. The data suggest that persistence of primed cells or generation of memory T cells may be compromised in these mice.

Publications

Original peer-reviewed articles

1.    Raman VS, Bal V, Rath S and George A (2000). Ligation of CD27 on murine B cells responding to T-dependent and T-independent stimuli inhibits the generation of plasma cells. J Immunol 165:6809-6815.

2.     Pasare C, Mukherjee P, Verhoef A, Bansal P, Mendiratta SK, George A, Lamb JR, Rath S and Bal V (2001) T cells in mice expressing a transgenic human T cell receptor b chain get positively selected but cannot be activated in the periphery by signaling through T cell receptor. Int Immunol 13:53-62.