HLA-E and NKG2A Mediate Resistance toM. bovisBCG Immunotherapy in Non-Muscle-Invasive Bladder Cancer

Author:

Ranti D.,Yu H.,Wang Y.A.,Bieber C.,Strandgaard T.,Salomé B.,Houghton Sean,Kim J.,Ravichandran H.,Okulate I.,Merritt E.,Bang S.,Demetriou A.,Li Z.,Lindskrog S. V.,Ruan D.F.,Daza J.,Rai R.,Hegewisch-Solloa E.,Mace E.M.ORCID,Fernandez-Rodriguez R.,Izadmehr S.,Doherty G.,Narasimhan A.,Farkas A.M.,Cruz-Encarnacion P.,Shroff S.,Patel F.,Tran M.,Park S.J.,Qi J.,Patel M.,Geanon D.,Kelly G.,de Real R.M.,Lee B.,Nie K.,Miake-Iye S.,Angeliadis K.,Radkevich E.,Thin T.H.,Garcia-Barros M.,Brown H.,Martin B.,Mateo A.,Soto A.,Sussman R.,Shiwlani S.,Francisco-Simon S.,Beaumont K.G.,Hu Y.,Wang Y-C.,Wang L.,Sebra R.P.,Smith S.,Skobe M.,Clancy-Thompson E.,Palmer D.,Hammond S.,Hopkins B. D.,Wiklund P.,Zhu J.,Bravo-Cordero J.J.,Brody R.,Hopkins B.,Chen Z.ORCID,Kim-Schulze S.,Dyrskjøt L.ORCID,Elemento O.,Tocheva A.,Song W-M.,Bhardwaj N.,Galsky M.D.,Sfakianos J.P.,Horowitz A.

Abstract

AbstractMycobacterium bovisBacillus Calmette-Guerin (BCG) is the primary treatment for non-muscle-invasive bladder cancer (NMIBC), known to stimulate inflammatory cytokines, notably interferon (IFN)-γ. We observed that prolonged IFN-γ exposure fosters adaptive resistance in recurrent tumors, aiding immune evasion and tumor proliferation. We identify HLA-E and NKG2A, part of a novel NK and T cell checkpoint pathway, as key mediators of resistance in BCG-unresponsive NMIBC. IFN-γ enhances HLA-E and PD-L1 expression in recurrent tumors, with an enrichment of intra-tumoral NKG2A-expressing NK and CD8 T cells. CXCL9+macrophages and dendritic cells and CXCL12-expressing stromal cells likely recruit CXCR3/CXCR4-expressing NK and T cells and CXCR7+HLA-EHIGHtumor cells. NK and CD8 T cells remain functional within BCG-unresponsive tumors but are inhibited by HLA-E and PD-L1, providing a framework for combined NKG2A and PD-L1 blockade strategy for bladder-sparing treatment of BCG-unresponsive NMIBC.

Publisher

Cold Spring Harbor Laboratory

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