T-cell Therapy for Progressive Multifocal Leukoencephalopathy
Sasha Gupta1, Tijana Martinov2, Ashley Thelen2, Megumi Sunahara1, Elaine Schanzer3, Fyodor Urnov3, Alexander Marson4, Brian Shy5, Philip Greenberg2, Michael Wilson6
1University of California, San Francisco, 2University of Washington, Fred Hutchinson Cancer Center, 3University of California, Berkeley; Innovative Genomics Institute, 4University of California, San Francisco; Gladstone Institute, 5University of California, San Francisco; Experimental Cellular Therapy, 6University of California San Francisco
Objective:
Create an “off-the-shelf” JC virus (JCV)-specific T cell therapy for progressive multifocal leukoencephalopathy (PML) patients who are immunocompromised and unable to adequately immune reconstitute.
Background:

PML is a fatal disease of the central nervous system caused by JCV. Survival is dependent on early diagnosis and ability to establish T cell immunity. Adoptive transfer of polyomavirus-specific T cells is possible; however, current delays in creating HLA-matched anti-viral T cells can be fatal.

Design/Methods:

PBMCs from healthy donors with specific HLA class I subtypes were stimulated with peptide libraries tiled across the JCV VP1 protein. Multiple rounds of stimulation were performed to identify the peptides that induced the largest CD8+ T cell activation (i.e., INFg, TNFa, CD137, and CD69 expression). For the immunogenic peptides antigens were narrowed and high-affinity antigen-specific CD8+ T cells were isolated using tetramers. Single-cell T cell receptor (TCR) sequencing identified high-affinity, VP1-specific TCR-a/b chain pairs. Candidate TCRs were then precisely introduced into the genome of T cells via CRISPR-Cas9 for further characterization.

Results:

A highly conserved region of the JCV VP1 protein (VP1100-108) was identified as an antigen for HLA-A2 CD8+ T cells with little potential for inducing autoimmunity. Fourteen high avidity TCRs specific for VP1100-108 were isolated, and ten demonstrated specific binding to VP1100-108 HLA-A2 tetramers. The top candidates have been integrated into T cells via CRISPR-Cas9 and are being further characterized. Other immunogenic regions of VP1 have been similarly identified for HLA-A1 and A3 alleles.   

Conclusions:

We identified immunogenic epitopes from the JCV VP1 protein that bind HLA-A1, A2, and A3 and isolated HLA-A2-restricted TCRs that demonstrated recognition and activation to the epitope of interest. While additional in vitro and in vivo validation is in progress, we believe these cells will offer a rapid, “off-the-shelf”, allogeneic anti-JCV T cell therapy for PML patients who are unable to immune reconstitute.

10.1212/WNL.0000000000204765