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B cells and tertiary lymphoid structures are associated with survival in papillary thyroid cancer

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Abstract

Purpose

The function of B cells in papillary thyroid cancer (PTC) is controversial. The role of B-cell-related tertiary lymphoid structures (TLSs) is still unclear. Whether B cells exert their anti-tumor effect through forming TLS in PTC needs further investigation.

Methods

We detected the percentage of B cells in PTC tissues by multi-parameter flow cytometry. Paraffin-embedded tumor tissues of 125 PTC patients were collected and stained with Haematoxylin–Eosin (H&E) for inflammatory infiltration analysis in combination with clinical features. Multiplexed immunohistochemistry (mIHC) was performed to verify the TLSs in above inflammatory infiltration. Correlation of B cells and TLSs with prognosis was analyzed using the TCGA database.

Results

We observed that PTC patients with higher expression of B lineage cell genes had improved survival and the percentage of B cells in the PTC tumor tissues was variable. Moreover, PTC tumor tissues with more B cells were surrounded by immune cell aggregates of varying sizes. We furtherly confirmed the immune cell aggregates as TLSs with different maturation stages. By analyzing PTC data from TCGA database, we found the maturation stages of TLSs were associated with genders and clinical stages among PTC patients. Moreover, patients with high TLSs survived longer and had a better prognosis.

Conclusion

B cells are associated with the existence of TLSs which have different maturation stages in PTC. Both B cells and TLSs are associated with the survival rate of PTC. These observations indicate that the anti-tumor effects of B cells in PTC are associated with TLSs formation.

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Data availability

Authors declare that the raw data supporting the conclusions of this article will be made available upon request.

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Funding

This work was supported by the Guangzhou Science and Technology Plan Project (202102080170 to B.X.), Project of Guangzhou Science and Technology Bureau (2023A03J0967 and 2023A03J0477), and the Program for Guangdong Introducing Innovative and Entrepreneurial Teams (2017ZT07S054).

Author information

Author notes

  1. Y.-Y. Li and S.-J. Li have contributed equally to this work and share first authorship.

Authors and Affiliations

  1. Department of Thyroid Surgery, the Second Affiliated Hospital, School of Medicine, South China University of Technology, Guangzhou, China

    Y.-Y. Li, S.-J. Li, Z. Chen, F. Shen & B. Xu

  2. School of Biomedical Sciences and Engineering, South China University of Technology, Guangzhou, China

    M.-C. Liu

  3. Medical Research Institute, Guangdong Provincial People’s Hospital (Guangdong Academy of Medical Sciences), Southern Medical University, Guangzhou, Guangdong, China

    L. Li

  4. Chronic Disease Laboratory, School of Medicine, South China University of Technology, Guangzhou, Guangdong, China

    Q.-Z. Liu

  5. Guangdong Provincial People’s Hospital (Guangdong Academy of Medical Sciences), Southern Medical University, Guangzhou, Guangdong, China

    Z.-X. Lian

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  1. Y.-Y. Li
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Contributions

Y-YL, S-JL and ZC: performed the experiments. Y-YL and S-JL: analyzed the data and plotted tables. FS: collected samples. M-CL: checked the data. LL, Q-ZL, BX and Z-XL: designed the work. BX: provided the funding of the project. YYL: wrote the manuscript. M-CL, LL, Q-ZL, BX and Z-XL: revised the manuscript.

Corresponding authors

Correspondence to Q.-Z. Liu or B. Xu.

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Conflict of interest

Authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Ethical approval

This study was approved by the Medical Ethics Committee of the Second Affiliated Hospital of South China University of Technology (K-2019-185). Written informed consent was obtained from all patients.

Informed consent

Informed consent was obtained from all individual participants included in the study.

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Li, YY., Li, SJ., Liu, MC. et al. B cells and tertiary lymphoid structures are associated with survival in papillary thyroid cancer. J Endocrinol Invest 46, 2247–2256 (2023). https://doi.org/10.1007/s40618-023-02072-w

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  • DOI: https://doi.org/10.1007/s40618-023-02072-w

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