Exploring breast tissue microbial composition and the association with breast cancer risk factors
Abstract Background Microbial dysbiosis has emerged as an important element in the development and progression of various cancers, including breast cancer. However, the microbial composition of the breast from healthy individuals, even relative to risk of developing breast cancer, remains unclear. H...
| Main Authors: | , , , , , , , , , |
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| Format: | Article |
| Language: | English |
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BMC
2023-07-01
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| Series: | Breast Cancer Research |
| Subjects: | |
| Online Access: | https://doi.org/10.1186/s13058-023-01677-6 |
| _version_ | 1797778650664271872 |
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| author | Rana German Natascia Marino Chris Hemmerich Ram Podicheti Douglas B. Rusch Leah T. Stiemsma Hongyu Gao Xiaoling Xuei Pam Rockey Anna Maria Storniolo |
| author_facet | Rana German Natascia Marino Chris Hemmerich Ram Podicheti Douglas B. Rusch Leah T. Stiemsma Hongyu Gao Xiaoling Xuei Pam Rockey Anna Maria Storniolo |
| author_sort | Rana German |
| collection | DOAJ |
| description | Abstract Background Microbial dysbiosis has emerged as an important element in the development and progression of various cancers, including breast cancer. However, the microbial composition of the breast from healthy individuals, even relative to risk of developing breast cancer, remains unclear. Here, we performed a comprehensive analysis of the microbiota of the normal breast tissue, which was analyzed in relation to the microbial composition of the tumor and adjacent normal tissue. Methods The study cohorts included 403 cancer-free women (who donated normal breast tissue cores) and 76 breast cancer patients (who donated tumor and/or adjacent normal tissue samples). Microbiome profiling was obtained by sequencing the nine hypervariable regions of the 16S rRNA gene (V1V2, V2V3, V3V4, V4V5, V5V7, and V7V9). Transcriptome analysis was also performed on 190 normal breast tissue samples. Breast cancer risk score was assessed using the Tyrer-Cuzick risk model. Results The V1V2 amplicon sequencing resulted more suitable for the analysis of the normal breast microbiome and identified Lactobacillaceae (Firmicutes phylum), Acetobacterraceae, and Xanthomonadaceae (both Proteobacteria phylum) as the most abundant families in the normal breast. However, Ralstonia (Proteobacteria phylum) was more abundant in both breast tumors and histologically normal tissues adjacent to malignant tumors. We also conducted a correlation analysis between the microbiome and known breast cancer risk factors. Abundances of the bacterial taxa Acetotobacter aceti, Lactobacillus vini, Lactobacillus paracasei, and Xanthonomas sp. were associated with age (p < 0.0001), racial background (p < 0.0001), and parity (p < 0.0001). Finally, transcriptome analysis of normal breast tissues showed an enrichment in metabolism- and immune-related genes in the tissues with abundant Acetotobacter aceti, Lactobacillus vini, Lactobacillus paracasei, and Xanthonomas sp., whereas the presence of Ralstonia in the normal tissue was linked to dysregulation of genes involved in the carbohydrate metabolic pathway. Conclusions This study defines the microbial features of normal breast tissue, thus providing a basis to understand cancer-related dysbiosis. Moreover, the findings reveal that lifestyle factors can significantly affect the normal breast microbial composition. |
| first_indexed | 2024-03-12T23:19:38Z |
| format | Article |
| id | doaj.art-a184415248e346bf9a23c93523061146 |
| institution | Directory Open Access Journal |
| issn | 1465-542X |
| language | English |
| last_indexed | 2024-03-12T23:19:38Z |
| publishDate | 2023-07-01 |
| publisher | BMC |
| record_format | Article |
| series | Breast Cancer Research |
| spelling | doaj.art-a184415248e346bf9a23c935230611462023-07-16T11:32:00ZengBMCBreast Cancer Research1465-542X2023-07-0125112110.1186/s13058-023-01677-6Exploring breast tissue microbial composition and the association with breast cancer risk factorsRana German0Natascia Marino1Chris Hemmerich2Ram Podicheti3Douglas B. Rusch4Leah T. Stiemsma5Hongyu Gao6Xiaoling Xuei7Pam Rockey8Anna Maria Storniolo9Susan G. Komen Tissue Bank at the IU Simon Comprehensive Cancer CenterSusan G. Komen Tissue Bank at the IU Simon Comprehensive Cancer CenterCenter for Genomics and Bioinformatics, Indiana UniversityCenter for Genomics and Bioinformatics, Indiana UniversityCenter for Genomics and Bioinformatics, Indiana UniversityNatural Science Division, Pepperdine UniversityDepartment of Medical and Molecular Genetics, Indiana University School of MedicineDepartment of Medical and Molecular Genetics, Indiana University School of MedicineSusan G. Komen Tissue Bank at the IU Simon Comprehensive Cancer CenterSusan G. Komen Tissue Bank at the IU Simon Comprehensive Cancer CenterAbstract Background Microbial dysbiosis has emerged as an important element in the development and progression of various cancers, including breast cancer. However, the microbial composition of the breast from healthy individuals, even relative to risk of developing breast cancer, remains unclear. Here, we performed a comprehensive analysis of the microbiota of the normal breast tissue, which was analyzed in relation to the microbial composition of the tumor and adjacent normal tissue. Methods The study cohorts included 403 cancer-free women (who donated normal breast tissue cores) and 76 breast cancer patients (who donated tumor and/or adjacent normal tissue samples). Microbiome profiling was obtained by sequencing the nine hypervariable regions of the 16S rRNA gene (V1V2, V2V3, V3V4, V4V5, V5V7, and V7V9). Transcriptome analysis was also performed on 190 normal breast tissue samples. Breast cancer risk score was assessed using the Tyrer-Cuzick risk model. Results The V1V2 amplicon sequencing resulted more suitable for the analysis of the normal breast microbiome and identified Lactobacillaceae (Firmicutes phylum), Acetobacterraceae, and Xanthomonadaceae (both Proteobacteria phylum) as the most abundant families in the normal breast. However, Ralstonia (Proteobacteria phylum) was more abundant in both breast tumors and histologically normal tissues adjacent to malignant tumors. We also conducted a correlation analysis between the microbiome and known breast cancer risk factors. Abundances of the bacterial taxa Acetotobacter aceti, Lactobacillus vini, Lactobacillus paracasei, and Xanthonomas sp. were associated with age (p < 0.0001), racial background (p < 0.0001), and parity (p < 0.0001). Finally, transcriptome analysis of normal breast tissues showed an enrichment in metabolism- and immune-related genes in the tissues with abundant Acetotobacter aceti, Lactobacillus vini, Lactobacillus paracasei, and Xanthonomas sp., whereas the presence of Ralstonia in the normal tissue was linked to dysregulation of genes involved in the carbohydrate metabolic pathway. Conclusions This study defines the microbial features of normal breast tissue, thus providing a basis to understand cancer-related dysbiosis. Moreover, the findings reveal that lifestyle factors can significantly affect the normal breast microbial composition.https://doi.org/10.1186/s13058-023-01677-6Normal breastLactobacillusAcetobacter acetiXanthomonas sp.RalstoniaBreast cancer risk factors |
| spellingShingle | Rana German Natascia Marino Chris Hemmerich Ram Podicheti Douglas B. Rusch Leah T. Stiemsma Hongyu Gao Xiaoling Xuei Pam Rockey Anna Maria Storniolo Exploring breast tissue microbial composition and the association with breast cancer risk factors Breast Cancer Research Normal breast Lactobacillus Acetobacter aceti Xanthomonas sp. Ralstonia Breast cancer risk factors |
| title | Exploring breast tissue microbial composition and the association with breast cancer risk factors |
| title_full | Exploring breast tissue microbial composition and the association with breast cancer risk factors |
| title_fullStr | Exploring breast tissue microbial composition and the association with breast cancer risk factors |
| title_full_unstemmed | Exploring breast tissue microbial composition and the association with breast cancer risk factors |
| title_short | Exploring breast tissue microbial composition and the association with breast cancer risk factors |
| title_sort | exploring breast tissue microbial composition and the association with breast cancer risk factors |
| topic | Normal breast Lactobacillus Acetobacter aceti Xanthomonas sp. Ralstonia Breast cancer risk factors |
| url | https://doi.org/10.1186/s13058-023-01677-6 |
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