Integrated metagenomics and transcriptomics analysis reveals pathways associated with oral periapical lesions formation and progression

Periapical abscesses, radicular cysts, and periapical granulomas are among the most frequently identified pathological lesions in the alveolar bone. Although many studies have investigated bacterial metagenomics in periapical abscesses, little is known about the genome mining of abundant bacteria in...

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Main Authors: Alaa Muayad Altaie, Thenmozhi Venkatachalam, Kiran Patil, Farah Al-Marzooq, Surendra Singh Rawat, Ali Al Qabbani, Mohammed Amjed Alsaegh, Lakshman P. Samaranayake, Sameh S.M. Soliman, Rifat Hamoudi
Format: Article
Language:English
Published: Elsevier 2025-01-01
Series:Current Research in Microbial Sciences
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Online Access:http://www.sciencedirect.com/science/article/pii/S266651742500104X
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author Alaa Muayad Altaie
Thenmozhi Venkatachalam
Kiran Patil
Farah Al-Marzooq
Surendra Singh Rawat
Ali Al Qabbani
Mohammed Amjed Alsaegh
Lakshman P. Samaranayake
Sameh S.M. Soliman
Rifat Hamoudi
author_facet Alaa Muayad Altaie
Thenmozhi Venkatachalam
Kiran Patil
Farah Al-Marzooq
Surendra Singh Rawat
Ali Al Qabbani
Mohammed Amjed Alsaegh
Lakshman P. Samaranayake
Sameh S.M. Soliman
Rifat Hamoudi
author_sort Alaa Muayad Altaie
collection DOAJ
description Periapical abscesses, radicular cysts, and periapical granulomas are among the most frequently identified pathological lesions in the alveolar bone. Although many studies have investigated bacterial metagenomics in periapical abscesses, little is known about the genome mining of abundant bacteria in periapical lesions and its correlation to human transcriptome. This study aims to explore the enriched metabolic environment of periapical lesions associated with microbial diversity and their role in lesion progression. Bacterial DNA and human RNA were isolated from periapical lesions and healthy pulp tissue and sequenced using next-generation sequencing (NGS). The sequences of the most abundant bacteria were then analyzed to identify secondary metabolites, pathogenic proteins, and their associated metabolic pathways. The results revealed that Fusobacterium nucleatum was the predominant bacterium in periapical abscesses and radicular cysts, whereas Porphyromonas endodontalis was the most abundant in periapical granulomas. Integrated bacterial and human metabolic pathways indicated that the augmentation of similar pathways is important in lesions pathogenesis. In periapical abscesses, inflammatory response, humoral immune response, positive regulation of cell migration, and hemopoiesis were enriched. In radicular cysts, pathways linked to NABA matrisome associated, inflammatory response, immune response-regulating signaling pathway, neutrophil degranulation, and P73 pathway were enriched. Meanwhile, periapical granulomas exhibited significant enrichment of pathways related to response to bacterium, regulation of immune effector process, and positive regulation of cell migration. In conclusion, this study is the first to elucidate the interplay between microbial and human metabolic activity associated with inflammation in abscesses, apoptosis in cysts, and inflammatory regulation in granulomas. These findings have significant clinical implications for the early diagnosis, prevention, and treatment of periapical lesions.
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spelling doaj-art-567f530e16414a45bc623358c19f28e12025-08-20T03:58:18ZengElsevierCurrent Research in Microbial Sciences2666-51742025-01-01910044310.1016/j.crmicr.2025.100443Integrated metagenomics and transcriptomics analysis reveals pathways associated with oral periapical lesions formation and progressionAlaa Muayad Altaie0Thenmozhi Venkatachalam1Kiran Patil2Farah Al-Marzooq3Surendra Singh Rawat4Ali Al Qabbani5Mohammed Amjed Alsaegh6Lakshman P. Samaranayake7Sameh S.M. Soliman8Rifat Hamoudi9Research Institute of Medical and Health Sciences, University of Sharjah, Sharjah P.O. Box 27272, United Arab Emirates; Center of Excellence for Precision Medicine, Research Institute of Medical and Health Sciences, University of Sharjah, Sharjah P.O. Box 27272, United Arab EmiratesDepartment of Biological Sciences, College of Medicine and Health Sciences, Khalifa University of Science and Technology, Abu Dhabi, P.O. Box 127788, United Arab EmiratesReference Laboratory for Infectious Disease, PureLab, Sheikh Khalifa Medical City, Abu Dhabi, United Arab EmiratesDepartment of Medical Microbiology and Immunology, College of Medicine and Health Sciences, UAE University, Al Ain, P.O. Box 15551, United Arab EmiratesDepartment of Research and Graduate Studies, College of Medicine and Health Sciences, Mohammed Bin Rashid University, Dubai, P.O. Box 505055, United Arab EmiratesDepartment of Oral and Craniofacial Health Sciences, College of Dental Medicine, University of Sharjah, Sharjah P.O. Box 27272, United Arab EmiratesDepartment of Oral and Craniofacial Health Sciences, College of Dental Medicine, University of Sharjah, Sharjah P.O. Box 27272, United Arab EmiratesDepartment of Oral Biosciences, Faculty of Dentistry, University of Hong Kong, Hong Kong; Global Research Cell, Dr. D. Y. Patil Dental College and Hospital, Dr. D. Y. Patil Vidyapeeth, Pimpri, Pune 411018, IndiaResearch Institute of Medical and Health Sciences, University of Sharjah, Sharjah P.O. Box 27272, United Arab Emirates; Department of Medicinal Chemistry, College of Pharmacy, University of Sharjah, Sharjah P.O. Box 27272, United Arab EmiratesResearch Institute of Medical and Health Sciences, University of Sharjah, Sharjah P.O. Box 27272, United Arab Emirates; Center of Excellence for Precision Medicine, Research Institute of Medical and Health Sciences, University of Sharjah, Sharjah P.O. Box 27272, United Arab Emirates; Department of Clinical Sciences, College of Medicine, University of Sharjah, Sharjah P.O. Box 27272, United Arab Emirates; BIMAI-Lab, Biomedically Informed Artificial Intelligence Laboratory, University of Sharjah, Sharjah P.O. Box 27272, United Arab Emirates; ASPIRE Precision Medicine Research Institute Abu Dhabi, University of Sharjah, Sharjah P.O. Box 27272, United Arab Emirates; Division of Surgery and Interventional Science, University College London, London, United Kingdom; Corresponding author.Periapical abscesses, radicular cysts, and periapical granulomas are among the most frequently identified pathological lesions in the alveolar bone. Although many studies have investigated bacterial metagenomics in periapical abscesses, little is known about the genome mining of abundant bacteria in periapical lesions and its correlation to human transcriptome. This study aims to explore the enriched metabolic environment of periapical lesions associated with microbial diversity and their role in lesion progression. Bacterial DNA and human RNA were isolated from periapical lesions and healthy pulp tissue and sequenced using next-generation sequencing (NGS). The sequences of the most abundant bacteria were then analyzed to identify secondary metabolites, pathogenic proteins, and their associated metabolic pathways. The results revealed that Fusobacterium nucleatum was the predominant bacterium in periapical abscesses and radicular cysts, whereas Porphyromonas endodontalis was the most abundant in periapical granulomas. Integrated bacterial and human metabolic pathways indicated that the augmentation of similar pathways is important in lesions pathogenesis. In periapical abscesses, inflammatory response, humoral immune response, positive regulation of cell migration, and hemopoiesis were enriched. In radicular cysts, pathways linked to NABA matrisome associated, inflammatory response, immune response-regulating signaling pathway, neutrophil degranulation, and P73 pathway were enriched. Meanwhile, periapical granulomas exhibited significant enrichment of pathways related to response to bacterium, regulation of immune effector process, and positive regulation of cell migration. In conclusion, this study is the first to elucidate the interplay between microbial and human metabolic activity associated with inflammation in abscesses, apoptosis in cysts, and inflammatory regulation in granulomas. These findings have significant clinical implications for the early diagnosis, prevention, and treatment of periapical lesions.http://www.sciencedirect.com/science/article/pii/S266651742500104XPeriapical lesionsMetagenomicsProteinsTranscriptomicsMetabolic pathwaysInflammation
spellingShingle Alaa Muayad Altaie
Thenmozhi Venkatachalam
Kiran Patil
Farah Al-Marzooq
Surendra Singh Rawat
Ali Al Qabbani
Mohammed Amjed Alsaegh
Lakshman P. Samaranayake
Sameh S.M. Soliman
Rifat Hamoudi
Integrated metagenomics and transcriptomics analysis reveals pathways associated with oral periapical lesions formation and progression
Current Research in Microbial Sciences
Periapical lesions
Metagenomics
Proteins
Transcriptomics
Metabolic pathways
Inflammation
title Integrated metagenomics and transcriptomics analysis reveals pathways associated with oral periapical lesions formation and progression
title_full Integrated metagenomics and transcriptomics analysis reveals pathways associated with oral periapical lesions formation and progression
title_fullStr Integrated metagenomics and transcriptomics analysis reveals pathways associated with oral periapical lesions formation and progression
title_full_unstemmed Integrated metagenomics and transcriptomics analysis reveals pathways associated with oral periapical lesions formation and progression
title_short Integrated metagenomics and transcriptomics analysis reveals pathways associated with oral periapical lesions formation and progression
title_sort integrated metagenomics and transcriptomics analysis reveals pathways associated with oral periapical lesions formation and progression
topic Periapical lesions
Metagenomics
Proteins
Transcriptomics
Metabolic pathways
Inflammation
url http://www.sciencedirect.com/science/article/pii/S266651742500104X
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