CXCL9:SPP1 macrophage polarity identifies a network of cellular programs that control human cancers

Tumor microenvironments (TMEs) influence cancer progression but are complex and often differ between patients. Considering that microenvironment variations may reveal rules governing intratumoral cellular programs and disease outcome, we focused on tumor-to-tumor variation to examine 52 head and nec...

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Published inScience (American Association for the Advancement of Science) Vol. 381; no. 6657; pp. 515 - 524
Main Authors Bill, Ruben, Wirapati, Pratyaksha, Messemaker, Marius, Roh, Whijae, Zitti, Beatrice, Duval, Florent, Kiss, Máté, Park, Jong Chul, Saal, Talia M., Hoelzl, Jan, Tarussio, David, Benedetti, Fabrizio, Tissot, Stéphanie, Kandalaft, Lana, Varrone, Marco, Ciriello, Giovanni, McKee, Thomas A., Monnier, Yan, Mermod, Maxime, Blaum, Emily M., Gushterova, Irena, Gonye, Anna L. K., Hacohen, Nir, Getz, Gad, Mempel, Thorsten R., Klein, Allon M., Weissleder, Ralph, Faquin, William C., Sadow, Peter M., Lin, Derrick, Pai, Sara I., Sade-Feldman, Moshe, Pittet, Mikael J.
Format Journal Article
LanguageEnglish
Published United States The American Association for the Advancement of Science 04.08.2023
Subjects
Cancer
Cell Polarity - immunology
Cellular communication
Chemokine CXCL9 - analysis
Chemokine CXCL9 - metabolism
Communication networks
Gene expression
Head & neck cancer
Head and neck carcinoma
Head and Neck Neoplasms - immunology
Head and Neck Neoplasms - pathology
Humans
Immune system
Immunotherapy
Macrophages
Macrophages - immunology
Microenvironments
Osteopontin - analysis
Osteopontin - metabolism
Patients
Polarity
Prognosis
Squamous cell carcinoma
Squamous Cell Carcinoma of Head and Neck - immunology
Squamous Cell Carcinoma of Head and Neck - pathology
Tumor Microenvironment
Tumors
Variation
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Abstract Tumor microenvironments (TMEs) influence cancer progression but are complex and often differ between patients. Considering that microenvironment variations may reveal rules governing intratumoral cellular programs and disease outcome, we focused on tumor-to-tumor variation to examine 52 head and neck squamous cell carcinomas. We found that macrophage polarity—defined by CXCL9 and SPP1 (CS) expression but not by conventional M1 and M2 markers—had a noticeably strong prognostic association. CS macrophage polarity also identified a highly coordinated network of either pro- or antitumor variables, which involved each tumor-associated cell type and was spatially organized. We extended these findings to other cancer indications. Overall, these results suggest that, despite their complexity, TMEs coordinate coherent responses that control human cancers and for which CS macrophage polarity is a relevant yet simple variable. One of the challenges in studying human disease is that the same condition can manifest differently across patients. However, patient variation can also be a positive thing, revealing information about the composition of diseased tissues and the relationship to disease outcome. Bill et al . used patient-to-patient variations to study how tumor microenvironments influence the progression of head and neck squamous cell carcinoma. The authors found that variations in macrophage polarity, defined by the expression of two genes, CXCL9 and SPP1 , was a simple but critical feature of tumor microenvironments. The CXCL9:SPP1 ratio could characterize the abundance of antitumor immune cells in cancer, gene expression programs in each tumor-infiltrating cell type, the regulation of communication networks that dictate tumor control or progression, and the response to immunotherapy. —Priscilla N. Kelly A two-gene signature from the tumor microenvironment of head and neck squamous cell carcinoma can predict tumor response to immunotherapy.
AbstractList Tumor microenvironments (TMEs) influence cancer progression but are complex and often differ between patients. Considering that microenvironment variations may reveal rules governing intratumoral cellular programs and disease outcome, we focused on tumor-to-tumor variation to examine 52 head and neck squamous cell carcinomas. We found that macrophage polarity-defined by CXCL9 and SPP1 (CS) expression but not by conventional M1 and M2 markers-had a noticeably strong prognostic association. CS macrophage polarity also identified a highly coordinated network of either pro- or antitumor variables, which involved each tumor-associated cell type and was spatially organized. We extended these findings to other cancer indications. Overall, these results suggest that, despite their complexity, TMEs coordinate coherent responses that control human cancers and for which CS macrophage polarity is a relevant yet simple variable.Tumor microenvironments (TMEs) influence cancer progression but are complex and often differ between patients. Considering that microenvironment variations may reveal rules governing intratumoral cellular programs and disease outcome, we focused on tumor-to-tumor variation to examine 52 head and neck squamous cell carcinomas. We found that macrophage polarity-defined by CXCL9 and SPP1 (CS) expression but not by conventional M1 and M2 markers-had a noticeably strong prognostic association. CS macrophage polarity also identified a highly coordinated network of either pro- or antitumor variables, which involved each tumor-associated cell type and was spatially organized. We extended these findings to other cancer indications. Overall, these results suggest that, despite their complexity, TMEs coordinate coherent responses that control human cancers and for which CS macrophage polarity is a relevant yet simple variable.
Editor’s summaryOne of the challenges in studying human disease is that the same condition can manifest differently across patients. However, patient variation can also be a positive thing, revealing information about the composition of diseased tissues and the relationship to disease outcome. Bill et al. used patient-to-patient variations to study how tumor microenvironments influence the progression of head and neck squamous cell carcinoma. The authors found that variations in macrophage polarity, defined by the expression of two genes, CXCL9 and SPP1, was a simple but critical feature of tumor microenvironments. The CXCL9:SPP1 ratio could characterize the abundance of antitumor immune cells in cancer, gene expression programs in each tumor-infiltrating cell type, the regulation of communication networks that dictate tumor control or progression, and the response to immunotherapy. —Priscilla N. Kelly
Tumor microenvironments (TMEs) influence cancer progression but are complex and often differ between patients. Considering that microenvironment variations may reveal rules governing intratumoral cellular programs and disease outcome, we focused on tumor-to-tumor variation to examine 52 head and neck squamous cell carcinomas. We found that macrophage polarity-defined by and (CS) expression but not by conventional M1 and M2 markers-had a noticeably strong prognostic association. CS macrophage polarity also identified a highly coordinated network of either pro- or antitumor variables, which involved each tumor-associated cell type and was spatially organized. We extended these findings to other cancer indications. Overall, these results suggest that, despite their complexity, TMEs coordinate coherent responses that control human cancers and for which CS macrophage polarity is a relevant yet simple variable.
Tumor microenvironments (TMEs) influence cancer progression but are complex and often differ between patients. Considering that microenvironment variations may reveal rules governing intratumoral cellular programs and disease outcome, we focused on tumor-to-tumor variation to examine 52 head and neck squamous cell carcinomas. We found that macrophage polarity—defined by CXCL9 and SPP1 (CS) expression but not by conventional M1 and M2 markers—had a noticeably strong prognostic association. CS macrophage polarity also identified a highly coordinated network of either pro- or antitumor variables, which involved each tumor-associated cell type and was spatially organized. We extended these findings to other cancer indications. Overall, these results suggest that, despite their complexity, TMEs coordinate coherent responses that control human cancers and for which CS macrophage polarity is a relevant yet simple variable. One of the challenges in studying human disease is that the same condition can manifest differently across patients. However, patient variation can also be a positive thing, revealing information about the composition of diseased tissues and the relationship to disease outcome. Bill et al . used patient-to-patient variations to study how tumor microenvironments influence the progression of head and neck squamous cell carcinoma. The authors found that variations in macrophage polarity, defined by the expression of two genes, CXCL9 and SPP1 , was a simple but critical feature of tumor microenvironments. The CXCL9:SPP1 ratio could characterize the abundance of antitumor immune cells in cancer, gene expression programs in each tumor-infiltrating cell type, the regulation of communication networks that dictate tumor control or progression, and the response to immunotherapy. —Priscilla N. Kelly A two-gene signature from the tumor microenvironment of head and neck squamous cell carcinoma can predict tumor response to immunotherapy.
Author Sadow, Peter M.
McKee, Thomas A.
Park, Jong Chul
Saal, Talia M.
Varrone, Marco
Tarussio, David
Bill, Ruben
Roh, Whijae
Messemaker, Marius
Pittet, Mikael J.
Kiss, Máté
Mermod, Maxime
Klein, Allon M.
Wirapati, Pratyaksha
Tissot, Stéphanie
Blaum, Emily M.
Mempel, Thorsten R.
Gushterova, Irena
Hacohen, Nir
Weissleder, Ralph
Zitti, Beatrice
Hoelzl, Jan
Faquin, William C.
Pai, Sara I.
Kandalaft, Lana
Benedetti, Fabrizio
Duval, Florent
Gonye, Anna L. K.
Lin, Derrick
Ciriello, Giovanni
Sade-Feldman, Moshe
Monnier, Yan
Getz, Gad
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  givenname: Jong Chul
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  organization: Department of Medicine, Massachusetts General Hospital and Harvard Medical School, Boston, MA, USA., Massachusetts General Hospital Cancer Center, Charlestown, MA, USA
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BackLink https://www.ncbi.nlm.nih.gov/pubmed/37535729$$D View this record in MEDLINE/PubMed
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Snippet Tumor microenvironments (TMEs) influence cancer progression but are complex and often differ between patients. Considering that microenvironment variations may...
Editor’s summaryOne of the challenges in studying human disease is that the same condition can manifest differently across patients. However, patient variation...
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StartPage 515
SubjectTerms Cancer
Cell Polarity - immunology
Cellular communication
Chemokine CXCL9 - analysis
Chemokine CXCL9 - metabolism
Communication networks
Gene expression
Head & neck cancer
Head and neck carcinoma
Head and Neck Neoplasms - immunology
Head and Neck Neoplasms - pathology
Humans
Immune system
Immunotherapy
Macrophages
Macrophages - immunology
Microenvironments
Osteopontin - analysis
Osteopontin - metabolism
Patients
Polarity
Prognosis
Squamous cell carcinoma
Squamous Cell Carcinoma of Head and Neck - immunology
Squamous Cell Carcinoma of Head and Neck - pathology
Tumor Microenvironment
Tumors
Variation
Title CXCL9:SPP1 macrophage polarity identifies a network of cellular programs that control human cancers
URI https://www.ncbi.nlm.nih.gov/pubmed/37535729
https://www.proquest.com/docview/2845173967
https://www.proquest.com/docview/2846931130
Volume 381
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