Oxidative Stress by H<sub>2</sub>O<sub>2</sub> as a Potential Inductor in the Switch from Commensal to Pathogen in Oncogenic Bacterium <i>Fusobacterium nucleatum</i>
Background: <i>Fusobacterium nucleatum</i> is a pathobiont that plays a dual role as both a commensal and a pathogen. The oral cavity typically harbors this anaerobic, Gram-negative bacterium. At the same time, it is closely linked to colorectal cancer due to its potential involvement in...
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MDPI AG
2025-03-01
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| Series: | Antioxidants |
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| Online Access: | https://www.mdpi.com/2076-3921/14/3/323 |
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| author | Alessandra Scano Sara Fais Giuliana Ciappina Martina Genovese Barbara Granata Monica Montopoli Pierluigi Consolo Patrizia Carroccio Paola Muscolino Alessandro Ottaiano Alessia Bignucolo Antonio Picone Enrica Toscano Germano Orrù Massimiliano Berretta |
| author_facet | Alessandra Scano Sara Fais Giuliana Ciappina Martina Genovese Barbara Granata Monica Montopoli Pierluigi Consolo Patrizia Carroccio Paola Muscolino Alessandro Ottaiano Alessia Bignucolo Antonio Picone Enrica Toscano Germano Orrù Massimiliano Berretta |
| author_sort | Alessandra Scano |
| collection | DOAJ |
| description | Background: <i>Fusobacterium nucleatum</i> is a pathobiont that plays a dual role as both a commensal and a pathogen. The oral cavity typically harbors this anaerobic, Gram-negative bacterium. At the same time, it is closely linked to colorectal cancer due to its potential involvement in tumor progression and resistance to chemotherapy. The mechanism by which it transforms from a commensal to a pathogen remains unknown. For this reason, we investigated the role of oxidative status as an initiatory factor in changing the bacterium’s pathogenicity profile. Methods: A clinical strain of <i>F. nucleatum</i> subsp. <i>animalis</i> biofilm was exposed to different oxidative stress levels through varying subinhibitory amounts of H<sub>2</sub>O<sub>2</sub>. Subsequently, we investigated the bacterium’s behavior in vitro by infecting the HT-29 cell line. We evaluated bacterial colonization, volatile sulfur compounds production, and the infected cell’s oxidative status by analyzing <i>HMOX1</i>, <i>pri-miRNA 155</i>, and <i>146a</i> gene expression. Results: The bacterial colonization rate, dimethyl sulfide production, and <i>pri-miRNA 155</i> levels all increased when stressed bacteria were used, suggesting a predominant pathogenic function of these strains. Conclusions: The response of <i>F. nucleatum</i> to different oxidative conditions could potentially explain the increase in its pathogenic traits and the existence of environmental factors that may trigger the bacterium’s pathogenicity and virulence. |
| format | Article |
| id | doaj-art-00aef80b579d45df8661e4525d64ebe7 |
| institution | DOAJ |
| issn | 2076-3921 |
| language | English |
| publishDate | 2025-03-01 |
| publisher | MDPI AG |
| record_format | Article |
| series | Antioxidants |
| spelling | doaj-art-00aef80b579d45df8661e4525d64ebe72025-08-20T02:42:35ZengMDPI AGAntioxidants2076-39212025-03-0114332310.3390/antiox14030323Oxidative Stress by H<sub>2</sub>O<sub>2</sub> as a Potential Inductor in the Switch from Commensal to Pathogen in Oncogenic Bacterium <i>Fusobacterium nucleatum</i>Alessandra Scano0Sara Fais1Giuliana Ciappina2Martina Genovese3Barbara Granata4Monica Montopoli5Pierluigi Consolo6Patrizia Carroccio7Paola Muscolino8Alessandro Ottaiano9Alessia Bignucolo10Antonio Picone11Enrica Toscano12Germano Orrù13Massimiliano Berretta14Oral Biotechnology Laboratory (OBL), Department of Surgical Science, University of Cagliari, 09124 Cagliari, ItalyOral Biotechnology Laboratory (OBL), Department of Surgical Science, University of Cagliari, 09124 Cagliari, ItalyDivision of Medical Oncology, AOU “G. Martino” Hospital, University of Messina, 98124 Messina, ItalyDepartment of Clinical and Experimental Medicine, University of Messina, 98122 Messina, ItalySchool of Specialization in Medical Oncology, Department of Human Pathology “G. Barresi”, University of Messina, 98125 Messina, ItalyDepartment of Pharmaceutical and Pharmacological Sciences, University of Padova, 35122 Padua, ItalyDepartment of Clinical and Experimental Medicine, University of Messina, 98122 Messina, ItalySchool of Specialization in Medical Oncology, Department of Human Pathology “G. Barresi”, University of Messina, 98125 Messina, ItalySchool of Specialization in Medical Oncology, Department of Human Pathology “G. Barresi”, University of Messina, 98125 Messina, ItalyDivision of Innovative Therapies for Abdominal Metastases, Istituto Nazionale Tumori IRCCS Fondazione G. Pascale, 80131 Naples, ItalyDepartment of Clinical and Experimental Medicine, University of Messina, 98122 Messina, ItalyDivision of Medical Oncology, AOU “G. Martino” Hospital, University of Messina, 98124 Messina, ItalySchool of Specialization in Medical Oncology, Department of Human Pathology “G. Barresi”, University of Messina, 98125 Messina, ItalyOral Biotechnology Laboratory (OBL), Department of Surgical Science, University of Cagliari, 09124 Cagliari, ItalyDivision of Medical Oncology, AOU “G. Martino” Hospital, University of Messina, 98124 Messina, ItalyBackground: <i>Fusobacterium nucleatum</i> is a pathobiont that plays a dual role as both a commensal and a pathogen. The oral cavity typically harbors this anaerobic, Gram-negative bacterium. At the same time, it is closely linked to colorectal cancer due to its potential involvement in tumor progression and resistance to chemotherapy. The mechanism by which it transforms from a commensal to a pathogen remains unknown. For this reason, we investigated the role of oxidative status as an initiatory factor in changing the bacterium’s pathogenicity profile. Methods: A clinical strain of <i>F. nucleatum</i> subsp. <i>animalis</i> biofilm was exposed to different oxidative stress levels through varying subinhibitory amounts of H<sub>2</sub>O<sub>2</sub>. Subsequently, we investigated the bacterium’s behavior in vitro by infecting the HT-29 cell line. We evaluated bacterial colonization, volatile sulfur compounds production, and the infected cell’s oxidative status by analyzing <i>HMOX1</i>, <i>pri-miRNA 155</i>, and <i>146a</i> gene expression. Results: The bacterial colonization rate, dimethyl sulfide production, and <i>pri-miRNA 155</i> levels all increased when stressed bacteria were used, suggesting a predominant pathogenic function of these strains. Conclusions: The response of <i>F. nucleatum</i> to different oxidative conditions could potentially explain the increase in its pathogenic traits and the existence of environmental factors that may trigger the bacterium’s pathogenicity and virulence.https://www.mdpi.com/2076-3921/14/3/323<i>Fusobacterium nucleatum</i>colon-rectal canceroxidative stresspri-miRNAgene expression |
| spellingShingle | Alessandra Scano Sara Fais Giuliana Ciappina Martina Genovese Barbara Granata Monica Montopoli Pierluigi Consolo Patrizia Carroccio Paola Muscolino Alessandro Ottaiano Alessia Bignucolo Antonio Picone Enrica Toscano Germano Orrù Massimiliano Berretta Oxidative Stress by H<sub>2</sub>O<sub>2</sub> as a Potential Inductor in the Switch from Commensal to Pathogen in Oncogenic Bacterium <i>Fusobacterium nucleatum</i> Antioxidants <i>Fusobacterium nucleatum</i> colon-rectal cancer oxidative stress pri-miRNA gene expression |
| title | Oxidative Stress by H<sub>2</sub>O<sub>2</sub> as a Potential Inductor in the Switch from Commensal to Pathogen in Oncogenic Bacterium <i>Fusobacterium nucleatum</i> |
| title_full | Oxidative Stress by H<sub>2</sub>O<sub>2</sub> as a Potential Inductor in the Switch from Commensal to Pathogen in Oncogenic Bacterium <i>Fusobacterium nucleatum</i> |
| title_fullStr | Oxidative Stress by H<sub>2</sub>O<sub>2</sub> as a Potential Inductor in the Switch from Commensal to Pathogen in Oncogenic Bacterium <i>Fusobacterium nucleatum</i> |
| title_full_unstemmed | Oxidative Stress by H<sub>2</sub>O<sub>2</sub> as a Potential Inductor in the Switch from Commensal to Pathogen in Oncogenic Bacterium <i>Fusobacterium nucleatum</i> |
| title_short | Oxidative Stress by H<sub>2</sub>O<sub>2</sub> as a Potential Inductor in the Switch from Commensal to Pathogen in Oncogenic Bacterium <i>Fusobacterium nucleatum</i> |
| title_sort | oxidative stress by h sub 2 sub o sub 2 sub as a potential inductor in the switch from commensal to pathogen in oncogenic bacterium i fusobacterium nucleatum i |
| topic | <i>Fusobacterium nucleatum</i> colon-rectal cancer oxidative stress pri-miRNA gene expression |
| url | https://www.mdpi.com/2076-3921/14/3/323 |
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