Analysis of antigen processing and presentation


 
Principal Investigator :   Satyajit Rath

Project Associates
Anjani Saxena
Deepa Rajagopal

Ph D Students
Sumeena Bhatia
Anita Garg
Ebenezer Chitra
Smita Srivastava
Ashutosh Chaudhry

Collaborators
Vineeta Bal
Jeannine M Durdik, Univ Arkansas, USA
Anna George
Satyajit Mayor, NCBS, Bangalore
B Ravindran, RMRC, Bhubaneswar
A Rudensky, Univ Washington, USA
Dinakar M Salunke
Ranjan Sen, Brandeis Univ, USA
Tushar Vaidya, CCMB, Hyderabad

The aim of the ongoing linked projects in this laboratory is to examine the generation and activation of T and B cells through a variety of linked experimental approaches.

A variety of experimental approaches are taken to address the theme issues. The approaches in current use examine APCs and pathways involved in antigen presentation to MHC class I and class II-restricted T cells; and analyse the consequences of intracellular signal transduction modulation for both, development and responses of B cells, T cells and macrophages using both genetic and pharmacological tools.

A.    Control of T cell memory commitment by autocrine free radicals

We have shown earlier that the cAMP-mediated pathway can activate specific commitment to long-term persistence of responsiveness during priming of human and mouse CD4 T cells in vitro and in vivo, probably by protecting activated T cells from apoptotic death through activation of protein kinase A (PKA)-I. However, blocking the cAMP-PKA pathway during normal priming of T cells does not modify either the induction of apoptosis or the efficiency of commitment to memory. Therefore, while the PKA-I pathway is a pharmacological mediator of T cell memory commitment, it does not normally operate in this context. In order to examine the apoptotic pathways which determine the normal limit to the induction of T cell memory, we have begun an investigation of the various potential mechanisms that can possibly mediate the death signal in activated T cells with respect to their relevance in T cell memory commitment.

Neither caspase inhibition nor Fas-FasL blockade could modify the efficiency of commitment of responding T cells to secondary responsiveness against alloantigenic target cells. The primary proliferative T cell responses were unaffected by these agents, but the secondary T cell proliferative responses were in fact enhanced, suggesting that Fas- and caspase-mediated death pathways could limit the actual responses mounted by secondary T cells, but may not play a major role in the determination of the memory T cell pool size during priming. On the other hand, MnTBAP, a metalloporphyrin known to be a mimic of SOD and peroxidase as well as a peroxynitrite inhibitor, could efficiently enhance T cell priming in vitro. However, it is not clear if secondary proliferative responses of T cells in vitro can be taken to reflect immune memory. We therefore examined if MnTBAP could induce any physiologically relevant modulation of immune T cell memory in vivo. Antigen-recalled T cell proliferative responses were enhanced if immunisation was done under cover of a five-day treatment with MnTBAP in vivo.

MnTBAP did not inhibit induction of primary T cell proliferation, unlike the cAMP pathway. However, it was efficient in blocking the induction of T cell activation-induced cell death (AICD) in vitro. Thus, MnTBAP treatment early during immunisation generates longer lasting T cell memory in vivo by inhibiting AICD-mediated T cell loss rather than inhibiting T cell activation per se.

It was not clear if MnTBAP was acting via the APCs or directly on T cells. We approached this issue by light fixation of the APCs used for priming alloresponses in vitro. Despite the inability of the fixed APCs to undergo any activation, the presence of MnTBAP led to enhanced T cell commitment to secondary responsiveness, indicating that its memory-enhancing effect was mediated directly on the T cells. Thus, it appears that autocrine free radical-mediated AICD may be crucial in limiting the degree of secondary responsiveness in antigen-responding primary T cell populations.

B.    Regulation of peptide-MHC complex generation and loss

Subunit vaccines consisting of peptidic epitopes have many advantages in terms of production and stability as well as precision of the triggered immune responses. However, effective immunogenicity of subunit vaccines has significant problems; - such small epitopic immunogens have short half-lives, and they need adjuvants. Long-lived peptides with high affinities for MHC may be able to ameliorate some of the difficulty. Further, increasing the longevity of antigen-specific peptide-MHC complexes on APCs in vivo increases their Th1 immunogenicity, which is useful for protection against intracellular pathogens, which are major public health problems, such as infections with Mycobacterium, Salmonella and Leishmania. Increasing the peptide-MHC complex density can be achieved by increasing the affinity of the peptide for the MHC molecule, and prolongation of the complex availability can be achieved by making the epitopes less susceptible to degradation. For both these possibilities, the structural basis of peptide mimic design needs to be established and tested in such systems, - an approach being used by our collaborators in structural biology. We have been using such designed non-degradable peptide mimics as antigens.

In such biological assays for peptide binding to MHC class I (MHCI), the retro-D forms of both an MHCI-binding peptide from ovalbumin (Oap) and an MHCI-binding peptide from a VSV glycoprotein (VSVp) bound well to the MHCI molecule, H-2K-b. The MHC-contacting residues of Oap that have been identified for the native L-form of the peptide were next tested in the retro-D form, and the residue dependence pattern was found to be similar, at least for two residues tested so far, supporting the prediction made in the analytical approach that the mode of interaction of retro-D peptides with MHC class I is similar to that of the native L-forms.

In the biological assays for recognition of these peptide-MHC complexes by T cells, the retro-D-Oap stimulated Oap-specific T cells very well. The D-mutations in the retro-D-Oap also stimulated the T cell line to the same extent that they could bind to H-2K-b, further supporting the similarities in binding and recognition of the two forms.

These studies were extended to the intracellular mechanisms for peptide loading on MHCI. L-Oap and retro-D-Oap were both loaded cytosolically by using the technique of osmotic lysis of pinosomes. While the presentation of L-Oap was dependent on the ABC-family peptide transporter TAP, the retro-D-Oap was well presented cytosolically independent of TAP. This suggested that the rate limiting factor for TAP-independent diffusional penetration of cytosolic peptides into the ER for MHC class I loading was likely to be the proteolytic degradation of the peptides in the cytosol. This was supported by the finding that proteasomal inhibitors allowed L-Oap also to be presented well cytosolically in a TAP-independent form.

Finally, the issue of the life-span of the peptide-MHC complexes on APCs was addressed by examining the half-life of either L-Oap or retro-D-Oap on APCs, and unequivocal data were obtained showing that retro-D-Oap survives for much longer periods than L-Oap does, supporting the speculation that this approach could modify the immunogenicity of peptidic antigens.

Publications

Original peer-reviewed articles

1.     Mukherjee P, Dani A, Bhatia S, Singh N, Rudensky AY, George A, Bal V, Mayor S and Rath S (2001) Efficient presentation of both cytosolic and endogenous transmembrane protein antigens on MHC class II is dependent on cytoplasmic proteolysis. J Immunol 167:2632-2641.

2.     Bhatia S, Mukhopadhyay S, Jarman E, Hall G, George A, Basu SK, Rath S, Lamb JR and Bal V (2002) Scavenger receptor-specific allergen delivery elicits IFN-g-dominated immunity and directs established TH2-dominated responses to a nonallergic phenotype. J Allergy Clin Immunol 109:321-328.

Miscellaneous

1.     Rath S (2001) Opportunities for science careers in India: an invitation to the Mad Hatter’s tea party. Economic & Political Weekly 36:1372.