Repressed <i>Blautia</i>-acetate immunological axis underlies breast cancer progression promoted by chronic stress

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Abstract

Chronic stress is a known risk factor for breast cancer, yet the underlying mechanisms are unclear. This study explores the potential involvement of microbial and metabolic signals in chronic stress-promoted breast cancer progression, revealing that reduced abundances of Blautia and its metabolite acetate may contribute to this process. Treatment with Blautia and acetate increases antitumor responses of CD8 ⁺ T cells and reverses stress-promoted breast cancer progression in female mice. Patients with depression exhibit lower abundances of Blautia and acetate, and breast cancer female patients with depression display lower abundances of acetate, decreased numbers of tumor-infiltrating CD8 ⁺ T cells, and an increased risk of metastasis. These results suggest that Blautia-derived acetate plays a crucial role in modulating the immune response to breast cancer, and its reduction may contribute to chronic stress-promoted cancer progression. Our findings advance the understanding of microbial and metabolic signals implicated in cancer in patients with depression and may provide therapeutic options for female patients with breast cancer and depression.

Abstract

Chronic stress can promote breast cancer progression. Here the authors show that a reduction in the levels of Blautia and its metabolite acetate contributes to chronic stress-promoted breast cancer progression, associated with decreased CD8 + T cell anti-tumor immunity.

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Global cancer statistics 2020: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries

Hyuna Sung, Jacques Ferlay, Rebecca Siegel … (2021)

This article provides an update on the global cancer burden using the GLOBOCAN 2020 estimates of cancer incidence and mortality produced by the International Agency for Research on Cancer. Worldwide, an estimated 19.3 million new cancer cases (18.1 million excluding nonmelanoma skin cancer) and almost 10.0 million cancer deaths (9.9 million excluding nonmelanoma skin cancer) occurred in 2020. Female breast cancer has surpassed lung cancer as the most commonly diagnosed cancer, with an estimated 2.3 million new cases (11.7%), followed by lung (11.4%), colorectal (10.0 %), prostate (7.3%), and stomach (5.6%) cancers. Lung cancer remained the leading cause of cancer death, with an estimated 1.8 million deaths (18%), followed by colorectal (9.4%), liver (8.3%), stomach (7.7%), and female breast (6.9%) cancers. Overall incidence was from 2-fold to 3-fold higher in transitioned versus transitioning countries for both sexes, whereas mortality varied <2-fold for men and little for women. Death rates for female breast and cervical cancers, however, were considerably higher in transitioning versus transitioned countries (15.0 vs 12.8 per 100,000 and 12.4 vs 5.2 per 100,000, respectively). The global cancer burden is expected to be 28.4 million cases in 2040, a 47% rise from 2020, with a larger increase in transitioning (64% to 95%) versus transitioned (32% to 56%) countries due to demographic changes, although this may be further exacerbated by increasing risk factors associated with globalization and a growing economy. Efforts to build a sustainable infrastructure for the dissemination of cancer prevention measures and provision of cancer care in transitioning countries is critical for global cancer control.

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Cancer statistics, 2023

Rebecca L Siegel, Kimberly D Miller, Nikita Sandeep Wagle … (2023)

Each year, the American Cancer Society estimates the numbers of new cancer cases and deaths in the United States and compiles the most recent data on population-based cancer occurrence and outcomes using incidence data collected by central cancer registries and mortality data collected by the National Center for Health Statistics. In 2023, 1,958,310 new cancer cases and 609,820 cancer deaths are projected to occur in the United States. Cancer incidence increased for prostate cancer by 3% annually from 2014 through 2019 after two decades of decline, translating to an additional 99,000 new cases; otherwise, however, incidence trends were more favorable in men compared to women. For example, lung cancer in women decreased at one half the pace of men (1.1% vs. 2.6% annually) from 2015 through 2019, and breast and uterine corpus cancers continued to increase, as did liver cancer and melanoma, both of which stabilized in men aged 50 years and older and declined in younger men. However, a 65% drop in cervical cancer incidence during 2012 through 2019 among women in their early 20s, the first cohort to receive the human papillomavirus vaccine, foreshadows steep reductions in the burden of human papillomavirus-associated cancers, the majority of which occur in women. Despite the pandemic, and in contrast with other leading causes of death, the cancer death rate continued to decline from 2019 to 2020 (by 1.5%), contributing to a 33% overall reduction since 1991 and an estimated 3.8 million deaths averted. This progress increasingly reflects advances in treatment, which are particularly evident in the rapid declines in mortality (approximately 2% annually during 2016 through 2020) for leukemia, melanoma, and kidney cancer, despite stable/increasing incidence, and accelerated declines for lung cancer. In summary, although cancer mortality rates continue to decline, future progress may be attenuated by rising incidence for breast, prostate, and uterine corpus cancers, which also happen to have the largest racial disparities in mortality.

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Transcript-level expression analysis of RNA-seq experiments with HISAT, StringTie and Ballgown

Mihaela Pertea, Daehwan Kim, Geo M Pertea … (2018)

High-throughput sequencing of messenger RNA (RNA-seq) has become the standard method for measuring and comparing the levels of gene expression in a wide variety of species and conditions. RNA-seq experiments generate very large, complex data sets that demand fast, accurate, and flexible software to reduce the raw read data to comprehensible results. HISAT, StringTie, and Ballgown are free, open-source software tools for comprehensive analysis of RNA-seq experiments. Together, they allow scientists to align reads to a genome, assemble transcripts including novel splice variants, compute the abundance of these transcripts in each sample, and compare experiments to identify differentially expressed genes and transcripts. This protocol describes all the steps necessary to process a large set of raw sequencing reads and create lists of gene transcripts, expression levels, and differentially expressed genes and transcripts. The protocol’s execution time depends on the computing resources, but typically takes under 45 minutes of computer time. Pertea et al. describe a protocol to analyze RNA-seq data using HISAT, StringTie, and Ballgown (the “new Tuxedo” package). The protocol can be used for assembly of transcripts, quantification of gene expression levels and differential expression analysis.

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Author and article information

Contributors

Guangyu Yao:

ORCID: http://orcid.org/0000-0002-3406-7612

yaogy@smu.edu.cn

Haiping Hao:

ORCID: http://orcid.org/0000-0003-2522-7546

haipinghao@cpu.edu.cn

Journal

Journal ID (nlm-ta): Nat Commun

Journal ID (iso-abbrev): Nat Commun

Title: Nature Communications

Publisher: Nature Publishing Group UK (London )

ISSN (Electronic): 2041-1723

Publication date (Electronic): 3 October 2023

Publication date PMC-release: 3 October 2023

Publication date Collection: 2023

Volume: 14

Electronic Location Identifier: 6160

Affiliations

[1 ]NMPA Key Laboratory for Research and Evaluation of Drug Metabolism, Guangdong Provincial Key Laboratory of New Drug Screening, School of Pharmaceutical Sciences, Southern Medical University, ( https://ror.org/01vjw4z39) Guangzhou, 510515 China

[2 ]State Key Laboratory of Natural Medicines, Jiangsu Province Key Laboratory of Drug Metabolism, China Pharmaceutical University, ( https://ror.org/01sfm2718) Nanjing, 210009 China

[3 ]Department of Pharmacy, Shenzhen Luohu People’s Hospital, ( https://ror.org/04bpt8p43) Shenzhen, 518000 China

[4 ]GRID grid.284723.8, ISNI 0000 0000 8877 7471, Department of Radiation Oncology, Nanfang Hospital, , Southern Medical University, ; Guangzhou, 510515 China

[5 ]GRID grid.284723.8, ISNI 0000 0000 8877 7471, Breast Center, Department of General Surgery, Nanfang Hospital, , Southern Medical University, ; Guangzhou, 510515 China

Author information

Ling Ye http://orcid.org/0000-0002-2012-7266

Hongmei Wang http://orcid.org/0000-0003-3269-8063

Qihan Zhang http://orcid.org/0009-0001-4899-1056

Qiaoli Feng http://orcid.org/0000-0002-6662-3118

Xiao Zheng http://orcid.org/0000-0002-3883-4372

Guangyu Yao http://orcid.org/0000-0002-3406-7612

Haiping Hao http://orcid.org/0000-0003-2522-7546

Article

Publisher ID: 41817

DOI: 10.1038/s41467-023-41817-2

PMC ID: 10547687

PubMed ID: 37789028

SO-VID: c1c66313-2da7-43d5-8653-13b8a8e04617

License:

Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/.

History

Date received : 20 April 2022

Date accepted : 20 September 2023

Funding

Funded by: the National Key Research and Development Programme of China

Funded by: FundRef https://doi.org/10.13039/501100002858, China Postdoctoral Science Foundation;

Award ID: 2021M693512

Award Recipient : Yuanlong Hou

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ScienceOpen disciplines: Uncategorized

Keywords: microbiome,depression,tumour immunology,breast cancer

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ScienceOpen disciplines: Uncategorized

Keywords: microbiome, depression, tumour immunology, breast cancer

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Repressed Blautia-acetate immunological axis underlies breast cancer progression promoted by chronic stress

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Karger: Oncology

Most cited references 64

Global cancer statistics 2020: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries

Cancer statistics, 2023

Transcript-level expression analysis of RNA-seq experiments with HISAT, StringTie and Ballgown

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Cited by 12

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