Intratumoral microbiome of adenoid cystic carcinomas and comparison with other head and neck cancers.
| Title: | Intratumoral microbiome of adenoid cystic carcinomas and comparison with other head and neck cancers. |
|---|---|
| Authors: | Karpinets TV; Department of Genomic Medicine, The University of Texas MD Anderson Cancer Center, Houston, TX, USA. tvkarpinets@mdanderson.org.; Mitani Y; Department of Pathology, The University of Texas MD Anderson Cancer Center, Houston, TX, USA.; Chang CC; Department of Genomic Medicine, The University of Texas MD Anderson Cancer Center, Houston, TX, USA.; Wu X; Department of Genomic Medicine, The University of Texas MD Anderson Cancer Center, Houston, TX, USA.; Song X; Department of Genomic Medicine, The University of Texas MD Anderson Cancer Center, Houston, TX, USA.; Flores II; Department of Genomic Medicine, The University of Texas MD Anderson Cancer Center, Houston, TX, USA.; McDaniel LK; Department of Genomic Medicine, The University of Texas MD Anderson Cancer Center, Houston, TX, USA.; Hoballah YM; Department of Genomic Medicine, The University of Texas MD Anderson Cancer Center, Houston, TX, USA.; Veguilla FJ; Department of Genomic Medicine, The University of Texas MD Anderson Cancer Center, Houston, TX, USA.; Ferrarotto R; Department of Thoracic/Head and Neck Medical Oncology, The University of Texas MD Anderson Cancer Center, Houston, TX, USA.; Colbert LE; Department of Radiation Oncology, The University of Texas MD Anderson Cancer Center, Houston, TX, USA.; Ajami NJ; Department of Genomic Medicine, The University of Texas MD Anderson Cancer Center, Houston, TX, USA.; Jenq RR; Department of Genomic Medicine, The University of Texas MD Anderson Cancer Center, Houston, TX, USA.; Zhang J; Department of Genomic Medicine, The University of Texas MD Anderson Cancer Center, Houston, TX, USA.; Futreal AP; Department of Genomic Medicine, The University of Texas MD Anderson Cancer Center, Houston, TX, USA.; El-Naggar AK; Department of Pathology, The University of Texas MD Anderson Cancer Center, Houston, TX, USA. |
| Source: | Scientific reports [Sci Rep] 2024 Jul 15; Vol. 14 (1), pp. 16300. Date of Electronic Publication: 2024 Jul 15. |
| Publication Type: | Journal Article; Comparative Study |
| Language: | English |
| Journal Info: | Publisher: Nature Publishing Group Country of Publication: England NLM ID: 101563288 Publication Model: Electronic Cited Medium: Internet ISSN: 2045-2322 (Electronic) Linking ISSN: 20452322 NLM ISO Abbreviation: Sci Rep Subsets: MEDLINE |
| Imprint Name(s): | Original Publication: London : Nature Publishing Group, copyright 2011- |
| MeSH Terms: | Carcinoma, Adenoid Cystic*/microbiology ; Carcinoma, Adenoid Cystic*/pathology ; Head and Neck Neoplasms*/microbiology ; Head and Neck Neoplasms*/pathology ; RNA, Ribosomal, 16S*/genetics ; Microbiota*; Bacteria/classification ; Bacteria/genetics ; Bacteria/isolation & purification ; Humans ; Female ; Male ; Middle Aged ; Aged ; Adult |
| Abstract: | Adenoid cystic carcinoma (ACC) is a rare, usually slow-growing yet aggressive head and neck malignancy. Despite its clinical significance, our understanding of the cellular evolution and microenvironment in ACC remains limited. We investigated the intratumoral microbiomes of 50 ACC tumor tissues and 33 adjacent normal tissues using 16S rRNA gene sequencing. This allowed us to characterize the bacterial communities within the ACC and explore potential associations between the bacterial community structure, patient clinical characteristics, and tumor molecular features obtained through RNA sequencing. The bacterial composition in the ACC was significantly different from that in adjacent normal salivary tissue, and the ACC exhibited diverse levels of species richness. We identified two main microbial subtypes within the ACC: oral-like and gut-like. Oral-like microbiomes, characterized by increased diversity and abundance of Neisseria, Leptotrichia, Actinomyces, Streptococcus, Rothia, and Veillonella (commonly found in healthy oral cavities), were associated with a less aggressive ACC-II molecular subtype and improved patient outcomes. Notably, we identified the same oral genera in oral cancer and head and neck squamous cell carcinomas. In both cancers, they were part of shared oral communities associated with a more diverse microbiome, less aggressive tumor phenotype, and better survival that reveal the genera as potential pancancer biomarkers for favorable microbiomes in ACC and other head and neck cancers. Conversely, gut-like intratumoral microbiomes, which feature low diversity and colonization by gut mucus layer-degrading species, such as Bacteroides, Akkermansia, Blautia, Bifidobacterium, and Enterococcus, were associated with poorer outcomes. Elevated levels of Bacteroides thetaiotaomicron were independently associated with significantly worse survival and positively correlated with tumor cell biosynthesis of glycan-based cell membrane components.; (© 2024. The Author(s).) |
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| Contributed Indexing: | Keywords: Bacteroides thetaiotaomicron; Bacterial; Mucus layer; Oral; Tumors |
| Substance Nomenclature: | 0 (RNA, Ribosomal, 16S) |
| Entry Date(s): | Date Created: 20240715 Date Completed: 20240715 Latest Revision: 20240801 |
| Update Code: | 20260130 |
| PubMed Central ID: | PMC11251153 |
| DOI: | 10.1038/s41598-024-65939-9 |
| PMID: | 39009605 |
| Database: | MEDLINE |
Journal Article; Comparative Study