bioRxiv Science⌕ Search

Biology subjects

Steele, M. M.

Publications and source records attributed to Steele, M. M..

3 recordsLinked to original sources

CXCR6 promotes dermal CD8+ T cell survival and transition to long-term tissue residence

Tissue resident memory T cells (TRM) provide protection against local re-infection, and yet the interstitial signals necessary for their formation and persistence remain incompletely understood. Here we show that antigen-dependent induction of the chemokine receptor, CXCR6, is a conserved adaptation to peripheral tissue infiltration that promotes TRM formation after viral infection. Deficient TRM formation in the absence of CXCR6 was not explained by canonical trafficking as CXCR6 was not required for tissue entry, was dispensable for the early accumulation of antigen-specific CD8+ T cells in skin, and did not restrain their exit. Further, single cell sequencing indicated that Cxcr6-/- CD8+ T cells were competent to acquire a transcriptional program of residence and TRM that formed were equally functional compared to their WT counterparts when reactivated greater than 100 days post primary infection. The reduced numbers observed at memory time points, where instead found to associate with impaired redox homeostasis and antioxidant capacity during the transition from effector to memory states. As such, Cxcr6-/- CD8+ T cells exhibited increased rates of apoptosis in the dermis relative to controls, which led to reduced numbers of TRM in the epidermis at memory. CXCR6 therefore promotes the metabolic adaptation of T cells as they engage antigen in tissue to increase the probability of memory differentiation and long-term residence. One Sentence SummaryCXCR6 promotes mechanisms of cellular adaptation to tissue that support local survival and the transition to tissue residence.

immunology↗

T cell Egress via Lymphatic Vessels Limits the Intratumoral T cell Repertoire in Melanoma

Antigen-specific CD8+ T cell accumulation in tumors is a prerequisite for effective immunotherapy, and yet, the mechanisms of lymphocyte transit remain poorly defined. We find that tumor-associated lymphatic vessels control T cell exit from tumors via the chemokine CXCL12, and intratumoral antigen encounter tunes CXCR4 expression on effector CD8+ T cells. Only high affinity antigen downregulates CXCR4 and upregulates the CXCL12 decoy receptor, ACKR3, thereby reducing CXCL12 sensitivity and promoting T cell retention. A diverse repertoire of functional tumor-specific CD8+ T cells exit the tumor, thereby limiting tumor control. CXCR4 inhibition and loss of lymphatic-specific CXCL12 boosts T cell retention and enhances response to therapeutic immune checkpoint blockade. Strategies that limit T cell egress, therefore, provide a new tool to boost immunotherapy response. One-Sentence SummaryLymphatic vessel-mediated, antigen-dependent CD8+ T cell egress limits T cell accumulation in melanomas and impairs anti-tumor immunity.

immunology↗

Infection-induced dermal lymphatic zippering restricts viral dissemination from skin and promotes anti-viral CD8+ T cell expansion.

Lymphatic vessels are often considered passive conduits that rapidly flush antigenic material, pathogens, and cells to draining lymph nodes. Recent evidence, however, suggests that lymphatic vessels actively regulate diverse processes from antigen transport to leukocyte trafficking and dietary lipid absorption. Here we tested the hypothesis that dermal lymphatic transport is dynamic and contributes to innate host defense during viral infection. We demonstrate that cutaneous vaccinia virus infection activates the tightening of lymphatic interendothelial junctions, termed zippering, in a VEGFA/VEGFR2-dependent manner. Both antibody-mediated blockade of VEGFA/VEGFR2 and lymphatic-specific deletion of Vegfr2 impaired lymphatic capillary zippering and increased fluid flux out of tissue. Strikingly, inhibition of lymphatic zippering allows viral dissemination to draining lymph nodes independent of dendritic cell migration and impairs CD8+ T cell priming. These data indicate that infection-induced dermal lymphatic capillary zippering is a context-dependent, active mechanism of innate host defense that limits interstitial fluid and virion flux and promotes protective, anti-viral CD8+ T cell responses. SummaryCutaneous infection with vaccinia virus induces VEGFR2-dependent dermal lymphatic capillary zippering. This tightening of lymphatic junctions exacerbates tissue edema, sequesters virus, and promotes anti-viral CD8+ T cell responses. Dermal lymphatic capillaries are therefore an active component of innate host defense.

immunology↗