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      Cancer stem cells promote lymph nodes metastasis of breast cancer by reprogramming tumor microenvironment

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          Highlights

          • •

            Breast cancer stem cells (CSCs) alter tumor immune microenvironment to promote lymph node metastasis.

          • •

            RAC2 and PTTG1 double-positive CSCs exhibit stem-like features and are enriched in metastatic lymph nodes.

          • •

            CSCs impact the evolution of adaptive and innate immune cells, contributing to metastasis progression.

          • •

            Findings provide insights for targeting therapy against highly stem-like CSCs in metastatic lymph nodes.

          • •

            Identification of RAC2 and PTTG1 double-positive CSCs provides new insights for developing targeted therapies.

          Abstract

          Breast cancer progression and metastasis are governed by a complex interplay within the tumor immune microenvironment (TIME), involving numerous cell types. Lymph node metastasis (LNM) is a key prognostic marker associated with distant organ metastasis and reduced patient survival, but the mechanisms underlying its promotion by breast cancer stem cells (CSCs) remain unclear. Our study sought to unravel how CSCs reprogram TIME to facilitate LNM. Utilizing single-cell RNA sequencing, we profiled TIME in primary cancer and corresponding metastatic lymph node samples from patients at our institution. To verify the derived data, we cultured CSCs and performed validation assays employing flow cytometry and CyTOF. Our analysis revealed distinct differences in cellular infiltration patterns between tumor and LNM samples. Importantly, RAC2 and PTTG1 double-positive CSCs, which exhibit the highest stem-like attributes, were markedly enriched in metastatic lymph nodes. These CSCs are hypothesized to foster metastasis via activation of specific metastasis-related transcription factors and signaling pathways. Additionally, our data suggest that CSCs might modulate adaptive and innate immune cell evolution, thereby further contributing to metastasis. In summary, this study illuminates a critical role of CSCs in modifying TIME to facilitate LNM. The enrichment of highly stem-like CSCs in metastatic lymph nodes offers novel therapeutic targeting opportunities and deepens our understanding of breast cancer metastasis.

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          Cancer statistics, 2019

          Rebecca Siegel, Kimberly D Miller, Ahmedin Jemal (2019)
          Each year, the American Cancer Society estimates the numbers of new cancer cases and deaths that will occur in the United States and compiles the most recent data on cancer incidence, mortality, and survival. Incidence data, available through 2015, were collected by the Surveillance, Epidemiology, and End Results Program; the National Program of Cancer Registries; and the North American Association of Central Cancer Registries. Mortality data, available through 2016, were collected by the National Center for Health Statistics. In 2019, 1,762,450 new cancer cases and 606,880 cancer deaths are projected to occur in the United States. Over the past decade of data, the cancer incidence rate (2006-2015) was stable in women and declined by approximately 2% per year in men, whereas the cancer death rate (2007-2016) declined annually by 1.4% and 1.8%, respectively. The overall cancer death rate dropped continuously from 1991 to 2016 by a total of 27%, translating into approximately 2,629,200 fewer cancer deaths than would have been expected if death rates had remained at their peak. Although the racial gap in cancer mortality is slowly narrowing, socioeconomic inequalities are widening, with the most notable gaps for the most preventable cancers. For example, compared with the most affluent counties, mortality rates in the poorest counties were 2-fold higher for cervical cancer and 40% higher for male lung and liver cancers during 2012-2016. Some states are home to both the wealthiest and the poorest counties, suggesting the opportunity for more equitable dissemination of effective cancer prevention, early detection, and treatment strategies. A broader application of existing cancer control knowledge with an emphasis on disadvantaged groups would undoubtedly accelerate progress against cancer.
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            Innate and adaptive immune cells in the tumor microenvironment.

            Thomas Gajewski, Hans Schreiber, Yang-Xin Fu (2013)
            Most tumor cells express antigens that can mediate recognition by host CD8(+) T cells. Cancers that are detected clinically must have evaded antitumor immune responses to grow progressively. Recent work has suggested two broad categories of tumor escape based on cellular and molecular characteristics of the tumor microenvironment. One major subset shows a T cell-inflamed phenotype consisting of infiltrating T cells, a broad chemokine profile and a type I interferon signature indicative of innate immune activation. These tumors appear to resist immune attack through the dominant inhibitory effects of immune system-suppressive pathways. The other major phenotype lacks this T cell-inflamed phenotype and appears to resist immune attack through immune system exclusion or ignorance. These two major phenotypes of tumor microenvironment may require distinct immunotherapeutic interventions for maximal therapeutic effect.
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              Breast cancer

              Nadia Harbeck, Michael Gnant (2017)
              Breast cancer is one of the three most common cancers worldwide. Early breast cancer is considered potentially curable. Therapy has progressed substantially over the past years with a reduction in therapy intensity, both for locoregional and systemic therapy; avoiding overtreatment but also undertreatment has become a major focus. Therapy concepts follow a curative intent and need to be decided in a multidisciplinary setting, taking molecular subtype and locoregional tumour load into account. Primary conventional surgery is not the optimal choice for all patients any more. In triple-negative and HER2-positive early breast cancer, neoadjuvant therapy has become a commonly used option. Depending on clinical tumour subtype, therapeutic backbones include endocrine therapy, anti-HER2 targeting, and chemotherapy. In metastatic breast cancer, therapy goals are prolongation of survival and maintaining quality of life. Advances in endocrine therapies and combinations, as well as targeting of HER2, and the promise of newer targeted therapies make the prospect of long-term disease control in metastatic breast cancer an increasing reality.
              Article 0 comments Cited 835 times – based on 0 reviews     Review now
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                Author and article information

                Contributors
                Zhigao Li
                Journal
                Journal ID (nlm-ta): Transl Oncol
                Journal ID (iso-abbrev): Transl Oncol
                Title: Translational Oncology
                Publisher: Neoplasia Press
                ISSN (Electronic): 1936-5233
                Publication date PMC-release: 06 July 2023
                Publication date Collection: September 2023
                Publication date (Electronic): 06 July 2023
                Volume: 35
                Electronic Location Identifier: 101733
                Affiliations
                [a ]Harbin Medical University Cancer Hospital, Harbin Medical University, No.150 Haping Rd, Nangang District, Harbin 150081, China
                [b ]Department of Pathology, Harbin Medical University, Harbin, China
                Author notes
                [* ]Corresponding author. drzhigaoli@ 123456hrbmu.edu.cn
                [1]

                These authors contributed the same to the article.

                Article
                Publisher Item ID: S1936-5233(23)00119-5 Publisher ID: 101733
                DOI: 10.1016/j.tranon.2023.101733
                PMC ID: 10339262
                PubMed ID: 37421907
                SO-VID: 2e127340-85bc-4bb5-91fc-8e944bed519f
                Copyright © © 2023 The Authors. Published by Elsevier Inc.
                License:

                This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).

                History
                Date received : 28 April 2023
                Date revision received : 1 June 2023
                Date accepted : 22 June 2023
                Categories
                Subject: Commentary

                Keywords: breast cancer 1,cancer stem cells (cscs) 2,tumor immune microenvironment (time) 3,single-cell rna sequencing (scrna-seq) 4,lymph node metastasis 5
                Data availability:
                Keywords: breast cancer 1, cancer stem cells (cscs) 2, tumor immune microenvironment (time) 3, single-cell rna sequencing (scrna-seq) 4, lymph node metastasis 5

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