Parvimonas micra, an oral pathobiont associated with colorectal cancer, epigenetically reprograms human colonocytes
ABSTRACTRecently, an intestinal dysbiotic microbiota with enrichment in oral cavity bacteria has been described in colorectal cancer (CRC) patients. Here, we characterize and investigate one of these oral pathobionts, the Gram-positive anaerobic coccus Parvimonas micra. We identified two phylotypes...
| Main Authors: | , , , , , , , , , , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
Taylor & Francis Group
2023-12-01
|
| Series: | Gut Microbes |
| Subjects: | |
| Online Access: | https://www.tandfonline.com/doi/10.1080/19490976.2023.2265138 |
| _version_ | 1797320572562046976 |
|---|---|
| author | Emma Bergsten Denis Mestivier Francoise Donnadieu Thierry Pedron Caroline Barau Landry Tsoumtsa Meda Amel Mettouchi Emmanuel Lemichez Olivier Gorgette Mathias Chamaillard Amaury Vaysse Stevenn Volant Abiba Doukani Philippe J. Sansonetti Iradj Sobhani Giulia Nigro |
| author_facet | Emma Bergsten Denis Mestivier Francoise Donnadieu Thierry Pedron Caroline Barau Landry Tsoumtsa Meda Amel Mettouchi Emmanuel Lemichez Olivier Gorgette Mathias Chamaillard Amaury Vaysse Stevenn Volant Abiba Doukani Philippe J. Sansonetti Iradj Sobhani Giulia Nigro |
| author_sort | Emma Bergsten |
| collection | DOAJ |
| description | ABSTRACTRecently, an intestinal dysbiotic microbiota with enrichment in oral cavity bacteria has been described in colorectal cancer (CRC) patients. Here, we characterize and investigate one of these oral pathobionts, the Gram-positive anaerobic coccus Parvimonas micra. We identified two phylotypes (A and B) exhibiting different phenotypes and adhesion capabilities. We observed a strong association of phylotype A with CRC, with its higher abundance in feces and in tumoral tissue compared with the normal homologous colonic mucosa, which was associated with a distinct methylation status of patients. By developing an in vitro hypoxic co-culture system of human primary colonic cells with anaerobic bacteria, we show that P. micra phylotype A alters the DNA methylation profile promoters of key tumor-suppressor genes, oncogenes, and genes involved in epithelial–mesenchymal transition. In colonic mucosa of CRC patients carrying P. micra phylotype A, we found similar DNA methylation alterations, together with significant enrichment of differentially expressed genes in pathways involved in inflammation, cell adhesion, and regulation of actin cytoskeleton, providing evidence of P. micra’s possible role in the carcinogenic process. |
| first_indexed | 2024-03-08T04:41:07Z |
| format | Article |
| id | doaj.art-a53bd29379ac48b9b5a182a0fab55a31 |
| institution | Directory Open Access Journal |
| issn | 1949-0976 1949-0984 |
| language | English |
| last_indexed | 2024-03-08T04:41:07Z |
| publishDate | 2023-12-01 |
| publisher | Taylor & Francis Group |
| record_format | Article |
| series | Gut Microbes |
| spelling | doaj.art-a53bd29379ac48b9b5a182a0fab55a312024-02-08T12:02:08ZengTaylor & Francis GroupGut Microbes1949-09761949-09842023-12-0115210.1080/19490976.2023.2265138Parvimonas micra, an oral pathobiont associated with colorectal cancer, epigenetically reprograms human colonocytesEmma Bergsten0Denis Mestivier1Francoise Donnadieu2Thierry Pedron3Caroline Barau4Landry Tsoumtsa Meda5Amel Mettouchi6Emmanuel Lemichez7Olivier Gorgette8Mathias Chamaillard9Amaury Vaysse10Stevenn Volant11Abiba Doukani12Philippe J. Sansonetti13Iradj Sobhani14Giulia Nigro15Unité de Pathogénie Microbienne Moléculaire, INSERM U1202, Institut Pasteur, Paris, FranceÉquipe universitaire EC2M3-EA7375, Université Paris- Est (UPEC), Créteil, FranceUnité de Pathogénie Microbienne Moléculaire, INSERM U1202, Institut Pasteur, Paris, FranceUnité de Pathogénie Microbienne Moléculaire, INSERM U1202, Institut Pasteur, Paris, FrancePlateforme de Ressources Biologiques, CHU Henri Mondor Assistance Publique Hôpitaux de Paris (APHP), Créteil, FranceUnité des Toxines Bactériennes, Université Paris Cité, CNRS UMR6047, INSERM U1306, Institut Pasteur, Paris, FranceUnité des Toxines Bactériennes, Université Paris Cité, CNRS UMR6047, INSERM U1306, Institut Pasteur, Paris, FranceUnité des Toxines Bactériennes, Université Paris Cité, CNRS UMR6047, INSERM U1306, Institut Pasteur, Paris, FrancePlateforme de Bio-Imagerie Ultrastructurale, Institut Pasteur, Université Paris Cité, Paris, FranceLaboratory of Cell Physiology, INSERM U1003, University of Lille, Lille, FranceBioinformatics and Biostatistics Hub, Institut Pasteur, Université Paris Cité, Paris, FranceBioinformatics and Biostatistics Hub, Institut Pasteur, Université Paris Cité, Paris, FranceSorbonne Université, Inserm, Unité Mixte de Service Production et Analyse de données en Sciences de la Vie et en Santé, Paris, FranceUnité de Pathogénie Microbienne Moléculaire, INSERM U1202, Institut Pasteur, Paris, FranceÉquipe universitaire EC2M3-EA7375, Université Paris- Est (UPEC), Créteil, FranceUnité de Pathogénie Microbienne Moléculaire, INSERM U1202, Institut Pasteur, Paris, FranceABSTRACTRecently, an intestinal dysbiotic microbiota with enrichment in oral cavity bacteria has been described in colorectal cancer (CRC) patients. Here, we characterize and investigate one of these oral pathobionts, the Gram-positive anaerobic coccus Parvimonas micra. We identified two phylotypes (A and B) exhibiting different phenotypes and adhesion capabilities. We observed a strong association of phylotype A with CRC, with its higher abundance in feces and in tumoral tissue compared with the normal homologous colonic mucosa, which was associated with a distinct methylation status of patients. By developing an in vitro hypoxic co-culture system of human primary colonic cells with anaerobic bacteria, we show that P. micra phylotype A alters the DNA methylation profile promoters of key tumor-suppressor genes, oncogenes, and genes involved in epithelial–mesenchymal transition. In colonic mucosa of CRC patients carrying P. micra phylotype A, we found similar DNA methylation alterations, together with significant enrichment of differentially expressed genes in pathways involved in inflammation, cell adhesion, and regulation of actin cytoskeleton, providing evidence of P. micra’s possible role in the carcinogenic process.https://www.tandfonline.com/doi/10.1080/19490976.2023.2265138Colorectal cancercolonic epithelial primary cellspathobiontsParvimonas micraDNA methylation |
| spellingShingle | Emma Bergsten Denis Mestivier Francoise Donnadieu Thierry Pedron Caroline Barau Landry Tsoumtsa Meda Amel Mettouchi Emmanuel Lemichez Olivier Gorgette Mathias Chamaillard Amaury Vaysse Stevenn Volant Abiba Doukani Philippe J. Sansonetti Iradj Sobhani Giulia Nigro Parvimonas micra, an oral pathobiont associated with colorectal cancer, epigenetically reprograms human colonocytes Gut Microbes Colorectal cancer colonic epithelial primary cells pathobionts Parvimonas micra DNA methylation |
| title | Parvimonas micra, an oral pathobiont associated with colorectal cancer, epigenetically reprograms human colonocytes |
| title_full | Parvimonas micra, an oral pathobiont associated with colorectal cancer, epigenetically reprograms human colonocytes |
| title_fullStr | Parvimonas micra, an oral pathobiont associated with colorectal cancer, epigenetically reprograms human colonocytes |
| title_full_unstemmed | Parvimonas micra, an oral pathobiont associated with colorectal cancer, epigenetically reprograms human colonocytes |
| title_short | Parvimonas micra, an oral pathobiont associated with colorectal cancer, epigenetically reprograms human colonocytes |
| title_sort | parvimonas micra an oral pathobiont associated with colorectal cancer epigenetically reprograms human colonocytes |
| topic | Colorectal cancer colonic epithelial primary cells pathobionts Parvimonas micra DNA methylation |
| url | https://www.tandfonline.com/doi/10.1080/19490976.2023.2265138 |
| work_keys_str_mv | AT emmabergsten parvimonasmicraanoralpathobiontassociatedwithcolorectalcancerepigeneticallyreprogramshumancolonocytes AT denismestivier parvimonasmicraanoralpathobiontassociatedwithcolorectalcancerepigeneticallyreprogramshumancolonocytes AT francoisedonnadieu parvimonasmicraanoralpathobiontassociatedwithcolorectalcancerepigeneticallyreprogramshumancolonocytes AT thierrypedron parvimonasmicraanoralpathobiontassociatedwithcolorectalcancerepigeneticallyreprogramshumancolonocytes AT carolinebarau parvimonasmicraanoralpathobiontassociatedwithcolorectalcancerepigeneticallyreprogramshumancolonocytes AT landrytsoumtsameda parvimonasmicraanoralpathobiontassociatedwithcolorectalcancerepigeneticallyreprogramshumancolonocytes AT amelmettouchi parvimonasmicraanoralpathobiontassociatedwithcolorectalcancerepigeneticallyreprogramshumancolonocytes AT emmanuellemichez parvimonasmicraanoralpathobiontassociatedwithcolorectalcancerepigeneticallyreprogramshumancolonocytes AT oliviergorgette parvimonasmicraanoralpathobiontassociatedwithcolorectalcancerepigeneticallyreprogramshumancolonocytes AT mathiaschamaillard parvimonasmicraanoralpathobiontassociatedwithcolorectalcancerepigeneticallyreprogramshumancolonocytes AT amauryvaysse parvimonasmicraanoralpathobiontassociatedwithcolorectalcancerepigeneticallyreprogramshumancolonocytes AT stevennvolant parvimonasmicraanoralpathobiontassociatedwithcolorectalcancerepigeneticallyreprogramshumancolonocytes AT abibadoukani parvimonasmicraanoralpathobiontassociatedwithcolorectalcancerepigeneticallyreprogramshumancolonocytes AT philippejsansonetti parvimonasmicraanoralpathobiontassociatedwithcolorectalcancerepigeneticallyreprogramshumancolonocytes AT iradjsobhani parvimonasmicraanoralpathobiontassociatedwithcolorectalcancerepigeneticallyreprogramshumancolonocytes AT giulianigro parvimonasmicraanoralpathobiontassociatedwithcolorectalcancerepigeneticallyreprogramshumancolonocytes |