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Association of <em>Fusobacterium nucleatum</em> with specific T-cell subsets in the colorectal carcinoma microenvironment

Borowsky, Jennifer; Haruki, Koichiro; Lau, Mai Chan; Costa, Andressa Dias; Väyrynen, Juha P.; Ugai, Tomotaka; Arima, Kota; da Silva, Annacarolina; Felt, Kristen D.; Zhao, Melissa; Gurjao, Carino; Twombly, Tyler S.; Fujiyoshi, Kenji; Väyrynen, Sara A.; Hamada, Tsuyoshi; Mima, Kosuke; Bullman, Susan; Harrison, Tabitha A.; Phipps, Amanda I.; Peters, Ulrike; Ng, Kimmie; Meyerhardt, Jeffrey A.; Song, Mingyang; Giovannucci, Edward L.; Wu, Kana; Zhang, Xuehong; Freeman, Gordon J.; Huttenhower, Curtis; Garrett, Wendy S.; Chan, Andrew T.; Leggett, Barbara A.; Whitehall, Vicki L. J.; Walker, Neal; Brown, Ian; Bettington, Mark; Nishihara, Reiko; Fuchs, Charles S.; Lennerz, Jochen K.; Giannakis, Marios; Nowak, Jonathan A.; Ogino, Shuji (2021-03-26)

 
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URL:
https://doi.org/10.1158/1078-0432.CCR-20-4009

Borowsky, Jennifer
Haruki, Koichiro
Lau, Mai Chan
Costa, Andressa Dias
Väyrynen, Juha P.
Ugai, Tomotaka
Arima, Kota
da Silva, Annacarolina
Felt, Kristen D.
Zhao, Melissa
Gurjao, Carino
Twombly, Tyler S.
Fujiyoshi, Kenji
Väyrynen, Sara A.
Hamada, Tsuyoshi
Mima, Kosuke
Bullman, Susan
Harrison, Tabitha A.
Phipps, Amanda I.
Peters, Ulrike
Ng, Kimmie
Meyerhardt, Jeffrey A.
Song, Mingyang
Giovannucci, Edward L.
Wu, Kana
Zhang, Xuehong
Freeman, Gordon J.
Huttenhower, Curtis
Garrett, Wendy S.
Chan, Andrew T.
Leggett, Barbara A.
Whitehall, Vicki L. J.
Walker, Neal
Brown, Ian
Bettington, Mark
Nishihara, Reiko
Fuchs, Charles S.
Lennerz, Jochen K.
Giannakis, Marios
Nowak, Jonathan A.
Ogino, Shuji
American Association for Cancer Research
26.03.2021

Borowsky, J., Haruki, K., Lau, M. C., Dias Costa, A., Väyrynen, J. P., Ugai, T., Arima, K., da Silva, A., Felt, K. D., Zhao, M., Gurjao, C., Twombly, T. S., Fujiyoshi, K., Väyrynen, S. A., Hamada, T., Mima, K., Bullman, S., Harrison, T. A., Phipps, A. I., … Ogino, S. (2021). Association of Fusobacterium nucleatum with Specific T-cell Subsets in the Colorectal Carcinoma Microenvironment. Clinical Cancer Research, 27(10), 2816–2826. https://doi.org/10.1158/1078-0432.ccr-20-4009

https://rightsstatements.org/vocab/InC/1.0/
© 2021 American Association for Cancer Research.
https://rightsstatements.org/vocab/InC/1.0/
doi:https://doi.org/10.1158/1078-0432.CCR-20-4009
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Julkaisun pysyvä osoite on
https://urn.fi/URN:NBN:fi-fe2021042611954
Tiivistelmä

Abstract

Purpose: While evidence indicates that Fusobacterium nucleatum (F. nucleatum) may promote colorectal carcinogenesis through its suppressive effect on T-cell–mediated antitumor immunity, the specific T-cell subsets involved remain uncertain.

Experimental Design: We measured F. nucleatum DNA within tumor tissue by quantitative PCR on 933 cases (including 128 F. nucleatum–positive cases) among 4,465 incident colorectal carcinoma cases in two prospective cohorts. Multiplex immunofluorescence combined with digital image analysis and machine learning algorithms for CD3, CD4, CD8, CD45RO (PTPRC isoform), and FOXP3 measured various T-cell subsets. We leveraged data on Bifidobacterium, microsatellite instability (MSI), tumor whole-exome sequencing, and M1/M2-type tumor-associated macrophages [TAM; by CD68, CD86, IRF5, MAF, and MRC1 (CD206) multimarker assay]. Using the 4,465 cancer cases and inverse probability weighting method to control for selection bias due to tissue availability, multivariable-adjusted logistic regression analysis assessed the association between F. nucleatum and T-cell subsets.

Results: The amount of F. nucleatum was inversely associated with tumor stromal CD3⁺ lymphocytes [multivariable OR, 0.47; 95% confidence interval (CI), 0.28–0.79, for F. nucleatum–high vs. -negative category; Ptrend = 0.0004] and specifically stromal CD3⁺CD4⁺CD45RO⁺ cells (corresponding multivariable OR, 0.52; 95% CI, 0.32–0.85; Ptrend = 0.003). These relationships did not substantially differ by MSI status, neoantigen load, or exome-wide tumor mutational burden. F. nucleatum was not significantly associated with tumor intraepithelial T cells or with M1 or M2 TAMs.

Conclusions: The amount of tissue F. nucleatum is associated with lower density of stromal memory helper T cells. Our findings provide evidence for the interactive pathogenic roles of microbiota and specific immune cells.

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