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Single-Cell Spatial Proteomics Analyses of Head and Neck Squamous Cell Carcinoma Reveal Tumor Heterogeneity and Immune Architectures Associated with Clinical Outcome

View ORCID ProfileKatie E. Blise, View ORCID ProfileShamilene Sivagnanam, Grace L. Banik, View ORCID ProfileLisa M. Coussens, View ORCID ProfileJeremy Goecks
doi: https://doi.org/10.1101/2021.03.10.434649
Katie E. Blise
aDepartment of Biomedical Engineering, Oregon Health & Science University, Portland, OR USA
bThe Knight Cancer Institute, Oregon Health & Science University, Portland, OR USA
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Shamilene Sivagnanam
bThe Knight Cancer Institute, Oregon Health & Science University, Portland, OR USA
cDepartment of Cell, Developmental & Cancer Biology, Oregon Health & Science University, Portland, OR USA
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Grace L. Banik
cDepartment of Cell, Developmental & Cancer Biology, Oregon Health & Science University, Portland, OR USA
dOtolaryngology-Head & Neck Surgery, Oregon Health & Science University, Portland, OR USA
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  • For correspondence: goecksj@ohsu.edu
Lisa M. Coussens
bThe Knight Cancer Institute, Oregon Health & Science University, Portland, OR USA
cDepartment of Cell, Developmental & Cancer Biology, Oregon Health & Science University, Portland, OR USA
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Jeremy Goecks
aDepartment of Biomedical Engineering, Oregon Health & Science University, Portland, OR USA
bThe Knight Cancer Institute, Oregon Health & Science University, Portland, OR USA
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  • For correspondence: goecksj@ohsu.edu
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ABSTRACT

There is increasing evidence that the spatial organization of cells within the tumor-immune microenvironment (TiME) of solid tumors influences survival and response to therapy in numerous cancer types. Here, we report results and demonstrate the applicability of quantitative single-cell spatial proteomics analyses in the TiME of primary and recurrent human papillomavirus (HPV)-negative head and neck squamous cell carcinoma (HNSCC) tumors. Single-cell compositions of a nine patient, primary and recurrent (n=18), HNSCC cohort is presented, followed by deeper investigation into the spatial architecture of the TiME and its relationship with clinical variables and progression free survival (PFS). Multiple spatial algorithms were used to quantify the spatial landscapes of immune cells within TiMEs and demonstrate that neoplastic tumor-immune cell spatial compartmentalization, rather than mixing, is associated with longer PFS. Mesenchymal (αSMA+) cellular neighborhoods describe distinct immune landscapes associated with neoplastic tumor-immune compartmentalization and improved patient outcomes. Results from this investigation are concordant with studies in other tumor types, suggesting that trends in TiME cellular heterogeneity and spatial organization may be shared across cancers and may provide prognostic value in multiple cancer types.

Competing Interest Statement

L.M. Coussens is a paid consultant for Cell Signaling Technologies, AbbVie Inc., and Shasqi Inc., received reagent and/or research support from Plexxikon Inc., Pharmacyclics, Inc., Acerta Pharma, LLC, Deciphera Pharmaceuticals, LLC, Genentech, Inc., Roche Glycart AG, Syndax Pharmaceuticals Inc., Innate Pharma, NanoString Technologies, and Cell Signaling Technologies, is a member of the Scientific Advisory Boards of Syndax Pharmaceuticals, Carisma Therapeutics, Zymeworks, Inc, Verseau Therapeutics, Cytomix Therapeutics, Inc., Hibercell., Inc., Alkermes, Inc., and Kineta Inc, and is a member of the Lustgarten Therapeutics Advisory working group. No potential conflicts of interest were disclosed by the other authors.

Footnotes

  • * Division of Otolaryngology, Children’s Hospital of Philadelphia, Philadelphia, PA USA

  • https://doi.org/10.5281/zenodo.5540356

  • https://github.com/kblise/HNSCC_mIHC_paper

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY 4.0 International license.
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Posted October 01, 2021.
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Single-Cell Spatial Proteomics Analyses of Head and Neck Squamous Cell Carcinoma Reveal Tumor Heterogeneity and Immune Architectures Associated with Clinical Outcome
Katie E. Blise, Shamilene Sivagnanam, Grace L. Banik, Lisa M. Coussens, Jeremy Goecks
bioRxiv 2021.03.10.434649; doi: https://doi.org/10.1101/2021.03.10.434649
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Single-Cell Spatial Proteomics Analyses of Head and Neck Squamous Cell Carcinoma Reveal Tumor Heterogeneity and Immune Architectures Associated with Clinical Outcome
Katie E. Blise, Shamilene Sivagnanam, Grace L. Banik, Lisa M. Coussens, Jeremy Goecks
bioRxiv 2021.03.10.434649; doi: https://doi.org/10.1101/2021.03.10.434649

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