B cell signatures and tertiary lymphoid structures contribute to outcome in head and neck squamous cell carcinoma

Ayana T. Ruffin, Anthony R. Cillo, Tracy Tabib, Angen Liu, Sayali Onkar, Sheryl R. Kunning, Caleb Lampenfeld, Huda I. Atiya, Irina Abecassis, Cornelius H. L. Kürten, Zengbiao Qi, Ryan Soose, Umamaheswar Duvvuri, Seungwon Kim, Steffi Oesterrich, Robert Lafyatis, Lan G. Coffman, Robert L. Ferris, Dario A. A. Vignali and Tullia C. Bruno ()
Additional contact information
Ayana T. Ruffin: University of Pittsburgh
Anthony R. Cillo: University of Pittsburgh
Tracy Tabib: University of Pittsburgh
Angen Liu: University of Pittsburgh
Sayali Onkar: University of Pittsburgh
Sheryl R. Kunning: University of Pittsburgh
Caleb Lampenfeld: University of Pittsburgh
Huda I. Atiya: Hillman Cancer Center
Irina Abecassis: University of Pittsburgh
Cornelius H. L. Kürten: University Duisburg-Essen
Zengbiao Qi: University of Pittsburgh
Ryan Soose: University of Pittsburgh
Umamaheswar Duvvuri: Hillman Cancer Center
Seungwon Kim: University of Pittsburgh
Steffi Oesterrich: Hillman Cancer Center
Robert Lafyatis: University of Pittsburgh
Lan G. Coffman: Hillman Cancer Center
Robert L. Ferris: University of Pittsburgh
Dario A. A. Vignali: University of Pittsburgh
Tullia C. Bruno: University of Pittsburgh

Nature Communications, 2021, vol. 12, issue 1, 1-16

Abstract: Abstract Current immunotherapy paradigms aim to reinvigorate CD8+ T cells, but the contribution of humoral immunity to antitumor immunity remains understudied. Here, we demonstrate that in head and neck squamous cell carcinoma (HNSCC) caused by human papillomavirus infection (HPV+), patients have transcriptional signatures of germinal center (GC) tumor infiltrating B cells (TIL-Bs) and spatial organization of immune cells consistent with tertiary lymphoid structures (TLS) with GCs, both of which correlate with favorable outcome. GC TIL-Bs in HPV+ HNSCC are characterized by distinct waves of gene expression consistent with dark zone, light zone and a transitional state of GC B cells. Semaphorin 4a expression is enhanced on GC TIL-Bs present in TLS of HPV+ HNSCC and during the differentiation of TIL-Bs. Our study suggests that therapeutics to enhance TIL-B responses in HNSCC should be prioritized in future studies to determine if they can complement current T cell mediated immunotherapies.

Date: 2021
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DOI: 10.1038/s41467-021-23355-x

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