Skip to content
1887

Abstract

Multiple reports have attempted to describe the tumour microbiota in head and neck cancer (HNSC).

However, these have failed to produce a consistent microbiota signature, which may undermine understanding the importance of bacterial-mediated effects in HNSC.

The aim of this study is to consolidate these datasets and identify a consensus microbiota signature in HNSC.

We analysed 12 published HNSC 16S rRNA microbial datasets collected from cancer, cancer-adjacent and non-cancer tissues to generate a consensus microbiota signature. These signatures were then validated using The Cancer Microbiome Atlas (TCMA) database and correlated with the tumour microenvironment phenotypes and patient’s clinical outcome.

We identified a consensus microbial signature at the genus level to differentiate between HNSC sample types, with cancer and cancer-adjacent tissues sharing more similarity than non-cancer tissues. Univariate analysis on 16S rRNA datasets identified significant differences in the abundance of 34 bacterial genera among the tissue types. Paired cancer and cancer-adjacent tissue analyses in 16S rRNA and TCMA datasets identified increased abundance in in cancer tissues and decreased abundance of , and in cancer-adjacent tissues. Furthermore, these bacteria were associated with different tumour microenvironment phenotypes. Notably, high signature was associated with high neutrophil (r=0.37, <0.0001), angiogenesis (r=0.38, <0.0001) and granulocyte signatures (r=0.38, <0.0001) and better overall patient survival [continuous: HR 0.8482, 95 % confidence interval (CI) 0.7758–0.9273, =0.0003].

Our meta-analysis demonstrates a consensus microbiota signature for HNSC, highlighting its potential importance in this disease.

Funding
This study was supported by the:
  • University of Adelaide (Award Postgraduate Research Scholarship)
    • Principle Award Recipient: LinhT.H. Mai
  • University of Adelaide (Award Postgraduate Research Scholarship)
    • Principle Award Recipient: FangmeinuoWu
  • University of Adelaide (Award Postgraduate Research Scholarship)
    • Principle Award Recipient: RunhaoLi
  • University of Adelaide (Award Postgraduate Research Scholarship)
    • Principle Award Recipient: KennyYeo
  • Garnett Passe and Rodney Williams Memorial Foundation (Award Senior Fellowship)
    • Principle Award Recipient: SarahVreugde
  • National Health and Medical Research Council (Award APP1196832)
    • Principle Award Recipient: Peter-JohnWormald
  • This is an open-access article distributed under the terms of the Creative Commons Attribution License. This article was made open access via a Publish and Read agreement between the Microbiology Society and the corresponding author’s institution.
Loading

Article metrics loading...

/content/journal/jmm/10.1099/jmm.0.001799
2024-02-01
2025-04-30
Loading full text...

Full text loading...

/deliver/fulltext/jmm/73/2/jmm001799.html?itemId=/content/journal/jmm/10.1099/jmm.0.001799&mimeType=html&fmt=ahah

References

  1. Dohlman AB, Arguijo Mendoza D, Ding S, Gao M, Dressman H et al. The cancer microbiome atlas: a pan-cancer comparative analysis to distinguish tissue-resident microbiota from contaminants. Cell Host Microbe 2021; 29:281–298 [View Article] [PubMed]
    [Google Scholar]
  2. Nejman D, Livyatan I, Fuks G, Gavert N, Zwang Y et al. The human tumor microbiome is composed of tumor type-specific intracellular bacteria. Science 2020; 368:973–980 [View Article] [PubMed]
    [Google Scholar]
  3. Xavier JB, Young VB, Skufca J, Ginty F, Testerman T et al. The cancer microbiome: distinguishing direct and indirect effects requires a systemic view. Trends Cancer 2020; 6:192–204 [View Article] [PubMed]
    [Google Scholar]
  4. Yang L, Li A, Wang Y, Zhang Y. Intratumoral microbiota: roles in cancer initiation, development and therapeutic efficacy. Signal Transduct Target Ther 2023; 8:35 [View Article] [PubMed]
    [Google Scholar]
  5. Vétizou M, Pitt JM, Daillère R, Lepage P, Waldschmitt N et al. Anticancer immunotherapy by CTLA-4 blockade relies on the gut microbiota. Science 2015; 350:1079–1084 [View Article] [PubMed]
    [Google Scholar]
  6. Sivan A, Corrales L, Hubert N, Williams JB, Aquino-Michaels K et al. Commensal Bifidobacterium promotes antitumor immunity and facilitates anti-PD-L1 efficacy. Science 2015; 350:1084–1089 [View Article] [PubMed]
    [Google Scholar]
  7. Fu A, Yao B, Dong T, Chen Y, Yao J et al. Tumor-resident intracellular microbiota promotes metastatic colonization in breast cancer. Cell 2022; 185:1356–1372 [View Article] [PubMed]
    [Google Scholar]
  8. Yu T, Guo F, Yu Y, Sun T, Ma D et al. Fusobacterium nucleatum promotes chemoresistance to colorectal cancer by modulating autophagy. Cell 2017; 170:548–563 [View Article] [PubMed]
    [Google Scholar]
  9. Spanogiannopoulos P, Kyaw TS, Guthrie BGH, Bradley PH, Lee JV et al. Host and gut bacteria share metabolic pathways for anti-cancer drug metabolism. Nat Microbiol 2022; 7:1605–1620 [View Article] [PubMed]
    [Google Scholar]
  10. Kalaora S, Nagler A, Nejman D, Alon M, Barbolin C et al. Identification of bacteria-derived HLA-bound peptides in melanoma. Nature 2021; 592:138–143 [View Article] [PubMed]
    [Google Scholar]
  11. Naghavian R, Faigle W, Oldrati P, Wang J, Toussaint NC et al. Microbial peptides activate tumour-infiltrating lymphocytes in glioblastoma. Nature 2023; 617:807–817 [View Article] [PubMed]
    [Google Scholar]
  12. Abed J, Emgård JEM, Zamir G, Faroja M, Almogy G et al. Fap2 mediates Fusobacterium nucleatum colorectal adenocarcinoma enrichment by binding to tumor-expressed gal-GalNAc. Cell Host Microbe 2016; 20:215–225 [View Article] [PubMed]
    [Google Scholar]
  13. Parhi L, Alon-Maimon T, Sol A, Nejman D, Shhadeh A et al. Breast cancer colonization by Fusobacterium nucleatum accelerates tumor growth and metastatic progression. Nat Commun 2020; 11:3259 [View Article] [PubMed]
    [Google Scholar]
  14. Gur C, Maalouf N, Shhadeh A, Berhani O, Singer BB et al. Fusobacterium nucleatum supresses anti-tumor immunity by activating CEACAM1. Oncoimmunology 2019; 8:e1581531 [View Article] [PubMed]
    [Google Scholar]
  15. Gur C, Ibrahim Y, Isaacson B, Yamin R, Abed J et al. Binding of the Fap2 protein of Fusobacterium nucleatum to human inhibitory receptor TIGIT protects tumors from immune cell attack. Immunity 2015; 42:344–355 [View Article] [PubMed]
    [Google Scholar]
  16. Yoon Y, Kim G, Jeon BN, Fang S, Park H. Bifidobacterium strain-specific rnhances the efficacy of cancer therapeutics in tumor-bearing mice. Cancers 2021; 13:957 [View Article] [PubMed]
    [Google Scholar]
  17. Asadollahi P, Ghanavati R, Rohani M, Razavi S, Esghaei M et al. Anti-cancer effects of Bifidobacterium species in colon cancer cells and a mouse model of carcinogenesis. PLoS One 2020; 15:e0232930 [View Article] [PubMed]
    [Google Scholar]
  18. Rossi T, Vergara D, Fanini F, Maffia M, Bravaccini S et al. Microbiota-derived metabolites in tumor progression and metastasis. Int J Mol Sci 2020; 21:16 [View Article] [PubMed]
    [Google Scholar]
  19. Krautkramer KA, Fan J, Bäckhed F. Gut microbial metabolites as multi-kingdom intermediates. Nat Rev Microbiol 2021; 19:77–94 [View Article] [PubMed]
    [Google Scholar]
  20. Bachem A, Makhlouf C, Binger KJ, de Souza DP, Tull D et al. Microbiota-derived short-chain fatty acids promote the memory potential of antigen-activated CD8+ T cells. Immunity 2019; 51:285–297 [View Article] [PubMed]
    [Google Scholar]
  21. Liang Y, Rao Z, Du D, Wang Y, Fang T. Butyrate prevents the migration and invasion, and aerobic glycolysis in gastric cancer via inhibiting Wnt/β-catenin/c-Myc signaling. Drug Dev Res 2023; 84:532–541 [View Article] [PubMed]
    [Google Scholar]
  22. Okumura S, Konishi Y, Narukawa M, Sugiura Y, Yoshimoto S et al. Gut bacteria identified in colorectal cancer patients promote tumourigenesis via butyrate secretion. Nat Commun 2021; 12:5674 [View Article] [PubMed]
    [Google Scholar]
  23. Zaiatz-Bittencourt V, Jones F, Tosetto M, Scaife C, Cagney G et al. Butyrate limits human natural killer cell effector function. Sci Rep 2023; 13:2715 [View Article] [PubMed]
    [Google Scholar]
  24. Bender MJ, McPherson AC, Phelps CM, Pandey SP, Laughlin CR et al. Dietary tryptophan metabolite released by intratumoral Lactobacillus reuteri facilitates immune checkpoint inhibitor treatment. Cell 2023; 186:1846–1862 [View Article] [PubMed]
    [Google Scholar]
  25. Tintelnot J, Xu Y, Lesker TR, Schönlein M, Konczalla L et al. Microbiota-derived 3-IAA influences chemotherapy efficacy in pancreatic cancer. Nature 2023; 615:168–174 [View Article] [PubMed]
    [Google Scholar]
  26. Orlandi E, Iacovelli NA, Tombolini V, Rancati T, Polimeni A et al. Potential role of microbiome in oncogenesis, outcome prediction and therapeutic targeting for head and neck cancer. Oral Oncol 2019; 99:104453 [View Article] [PubMed]
    [Google Scholar]
  27. Burcher KM, Burcher JT, Inscore L, Bloomer CH, Furdui CM et al. A review of the role of oral microbiome in the development, detection, and management of head and neck squamous cell cancers. Cancers 2022; 14:17 [View Article] [PubMed]
    [Google Scholar]
  28. Orlandi E, Iacovelli NA, Tombolini V, Rancati T, Polimeni A et al. Potential role of microbiome in oncogenesis, outcome prediction and therapeutic targeting for head and neck cancer. Oral Oncol 2019; 99:104453 [View Article]
    [Google Scholar]
  29. Jain V, Baraniya D, El-Hadedy DE, Chen T, Slifker M et al. Integrative metatranscriptomic analysis reveals disease-specific microbiome-host interactions in oral squamous cell carcinoma. Cancer Res Commun 2023; 3:807–820 [View Article] [PubMed]
    [Google Scholar]
  30. Qiao H, Li H, Wen X, Tan X, Yang C et al. Multi-omics integration reveals the crucial role of Fusobacterium in the inflammatory immune microenvironment in head and neck squamous cell carcinoma. Microbiol Spectr 2022; 10:e0106822 [View Article] [PubMed]
    [Google Scholar]
  31. Zhou J, Wang L, Yuan R, Yu X, Chen Z et al. Signatures of mucosal microbiome in oral squamous cell carcinoma identified using a random forest model. Cancer Manag Res 2020; 12:5353–5363 [View Article] [PubMed]
    [Google Scholar]
  32. Torralba MG, Aleti G, Li W, Moncera KJ, Lin Y-H et al. Oral microbial species and virulence factors associated with oral squamous cell carcinoma. Microb Ecol 2021; 82:1030–1046 [View Article] [PubMed]
    [Google Scholar]
  33. Chang C, Geng F, Shi X, Li Y, Zhang X et al. The prevalence rate of periodontal pathogens and its association with oral squamous cell carcinoma. Appl Microbiol Biotechnol 2019; 103:1393–1404 [View Article] [PubMed]
    [Google Scholar]
  34. Al-Hebshi NN, Nasher AT, Maryoud MY, Homeida HE, Chen T et al. Inflammatory bacteriome featuring Fusobacterium nucleatum and Pseudomonas aeruginosa identified in association with oral squamous cell carcinoma. Sci Rep 2017; 7:1834 [View Article] [PubMed]
    [Google Scholar]
  35. Sarkar P, Malik S, Laha S, Das S, Bunk S et al. Dysbiosis of oral microbiota during oral squamous cell carcinoma development. Front Oncol 2021; 11:614448 [View Article] [PubMed]
    [Google Scholar]
  36. Gopinath D, Menon RK, Wie CC, Banerjee M, Panda S et al. Differences in the bacteriome of swab, saliva, and tissue biopsies in oral cancer. Sci Rep 2021; 11:1181 [View Article] [PubMed]
    [Google Scholar]
  37. Yu X, Shi Y, Yuan R, Chen Z, Dong Q et al. Microbial dysbiosis in oral squamous cell carcinoma: a systematic review and meta-analysis. Heliyon 2023; 9:e13198 [View Article]
    [Google Scholar]
  38. Gopinath D, Menon RK, Banerjee M, Su Yuxiong R, Botelho MG et al. Culture-independent studies on bacterial dysbiosis in oral and oropharyngeal squamous cell carcinoma: a systematic review. Crit Rev Oncol Hematol 2019; 139:31–40 [View Article] [PubMed]
    [Google Scholar]
  39. Peter TK, Withanage MHH, Comnick CL, Pendleton C, Dabdoub S et al. Systematic review and meta-analysis of oral squamous cell carcinoma associated oral microbiome. Front Microbiol 2022; 13:968304 [View Article] [PubMed]
    [Google Scholar]
  40. Ting HSL, Chen Z, Chan JYK. Systematic review on oral microbial dysbiosis and its clinical associations with head and neck squamous cell carcinoma. Head & Neck 2023; 45:2120–2135 [View Article]
    [Google Scholar]
  41. Metsäniitty M, Hasnat S, Salo T, Salem A. Oral microbiota-a new frontier in the pathogenesis and management of head and neck cancers. Cancers 2021; 14:46 [View Article] [PubMed]
    [Google Scholar]
  42. Su Mun L, Wye Lum S, Kong Yuiin Sze G, Hock Yoong C, Ching Yung K et al. Association of microbiome with oral squamous cell carcinoma: a systematic review of the metagenomic studies. Int J Environ Res Public Health 2021; 18:14 [View Article] [PubMed]
    [Google Scholar]
  43. Ramos RT, Sodré CS, de Sousa Rodrigues PMGR, da Silva AMP, Fuly MS et al. High-throughput nucleotide sequencing for bacteriome studies in oral squamous cell carcinoma: a systematic review. Oral Maxillofac Surg 2020; 24:387–401 [View Article] [PubMed]
    [Google Scholar]
  44. Delaney C, Veena CLR, Butcher MC, McLean W, Shaban SMA et al. Limitations of using 16S rRNA microbiome sequencing to predict oral squamous cell carcinoma. APMIS 2023; 131:262–276 [View Article] [PubMed]
    [Google Scholar]
  45. Wang Y, Lê Cao K-A. PLSDA-batch: a multivariate framework to correct for batch effects in microbiome data. Brief Bioinform 2023; 24:bbac622 [View Article] [PubMed]
    [Google Scholar]
  46. Sterne JAC, Savović J, Page MJ, Elbers RG, Blencowe NS et al. RoB 2: a revised tool for assessing risk of bias in randomised trials. BMJ 2019l4898 [View Article]
    [Google Scholar]
  47. Choudhary S. pysradb: a python package to query next-generation sequencing metadata and data from NCBI Sequence Read Archive. F1000Res 2019; 8:532 [View Article]
    [Google Scholar]
  48. Leinonen R, Sugawara H, Shumway M. The sequence read archive. Nucleic Acids Res 2011; 39:D19–21 [View Article] [PubMed]
    [Google Scholar]
  49. Bolyen E, Rideout JR, Dillon MR, Bokulich NA, Abnet CC et al. Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2. Nat Biotechnol 2019; 37:852–857 [View Article]
    [Google Scholar]
  50. Rohart F, Gautier B, Singh A, Lê Cao K-A. mixOmics: an R package for omics feature selection and multiple data integration. PLoS Comput Biol 2017; 13:e1005752 [View Article] [PubMed]
    [Google Scholar]
  51. McMurdie PJ, Holmes S. phyloseq: an R package for reproducible interactive analysis and graphics of microbiome census data. PLoS One 2013; 8:e61217 [View Article] [PubMed]
    [Google Scholar]
  52. Gloor GB, Macklaim JM, Pawlowsky-Glahn V, Egozcue JJ. Microbiome datasets are compositional: and this is not optional. Front Microbiol 2017; 8:2224 [View Article] [PubMed]
    [Google Scholar]
  53. R Core Team R R: A language and environment for statistical computing; 2013
  54. Douglas GM, Maffei VJ, Zaneveld JR, Yurgel SN, Brown JR et al. PICRUSt2 for prediction of metagenome functions. Nat Biotechnol 2020; 38:685–688 [View Article]
    [Google Scholar]
  55. Gao J, Aksoy BA, Dogrusoz U, Dresdner G, Gross B et al. Integrative analysis of complex cancer genomics and clinical profiles using the cBioPortal. Sci Signal 2013; 6:pl1 [View Article] [PubMed]
    [Google Scholar]
  56. Bagaev A, Kotlov N, Nomie K, Svekolkin V, Gafurov A et al. Conserved pan-cancer microenvironment subtypes predict response to immunotherapy. Cancer Cell 2021; 39:845–865 [View Article] [PubMed]
    [Google Scholar]
  57. Zhou X, Hao Y, Peng X, Li B, Han Q et al. The clinical potential of oral microbiota as a screening tool for oral squamous cell carcinomas. Front Cell Infect Microbiol 2021; 11:728933 [View Article] [PubMed]
    [Google Scholar]
  58. Wang X, Zhao Z, Tang N, Zhao Y, Xu J et al. Microbial community analysis of saliva and biopsies in patients with oral lichen planus. Front Microbiol 2020; 11:629 [View Article]
    [Google Scholar]
  59. Chen Z, Wong PY, Ng CWK, Lan L, Fung S et al. The intersection between oral microbiota, host gene methylation and patient outcomes in head and neck squamous cell carcinoma. Cancers 2020; 12:3425 [View Article]
    [Google Scholar]
  60. Zakrzewski M, Gannon OM, Panizza BJ, Saunders NA, Antonsson A. Human papillomavirus infection and tumor microenvironment are associated with the microbiota in patients with oropharyngeal cancers-pilot study. Head Neck 2021; 43:3324–3330 [View Article] [PubMed]
    [Google Scholar]
  61. De Martin A, Lütge M, Stanossek Y, Engetschwiler C, Cupovic J et al. Distinct microbial communities colonize tonsillar squamous cell carcinoma. Oncoimmunology 2021; 10:1945202 [View Article] [PubMed]
    [Google Scholar]
  62. Zhang Z, Feng Q, Li M, Li Z, Xu Q et al. Age-related cancer-associated microbiota potentially promotes oral squamous cell cancer tumorigenesis by distinct mechanisms. Front Microbiol 2022; 13: [View Article]
    [Google Scholar]
  63. Nie F, Wang L, Huang Y, Yang P, Gong P et al. Characteristics of microbial distribution in different oral niches of oral squamous cell carcinoma. Front Cell Infect Microbiol 2022; 12:905653 [View Article] [PubMed]
    [Google Scholar]
  64. Gong H, Shi Y, Xiao X, Cao P, Wu C et al. Alterations of microbiota structure in the larynx relevant to laryngeal carcinoma. Sci Rep 2017; 7:5507 [View Article] [PubMed]
    [Google Scholar]
  65. Perera M, Al-Hebshi NN, Perera I, Ipe D, Ulett GC et al. Inflammatory bacteriome and oral squamous cell carcinoma. J Dent Res 2018; 97:725–732 [View Article] [PubMed]
    [Google Scholar]
  66. Gong H-L, Shi Y, Zhou L, Wu C-P, Cao P-Y et al. The composition of microbiome in larynx and the throat biodiversity between laryngeal squamous cell carcinoma patients and control population. PLoS One 2013; 8:e66476 [View Article] [PubMed]
    [Google Scholar]
  67. Dong Z, Zhang C, Zhao Q, Huangfu H, Xue X et al. Alterations of bacterial communities of vocal cord mucous membrane increases the risk for glottic laryngeal squamous cell carcinoma. J Cancer 2021; 12:4049–4063 [View Article] [PubMed]
    [Google Scholar]
  68. Shin JM, Luo T, Kamarajan P, Fenno JC, Rickard AH et al. Microbial communities associated with primary and metastatic head and neck squamous cell carcinoma - a high fusobacterial and low streptococcal signature. Sci Rep 2017; 7:9934 [View Article] [PubMed]
    [Google Scholar]
  69. Yang K, Wang Y, Zhang S, Zhang D, Hu L et al. Oral microbiota analysis of tissue pairs and saliva samples from patients with oral squamous cell carcinoma - a pilot study. Front Microbiol 2021; 12:719601 [View Article] [PubMed]
    [Google Scholar]
  70. Gong H, Shi Y, Zhou X, Wu C, Cao P et al. Microbiota in the throat and risk factors for laryngeal carcinoma. Appl Environ Microbiol 2014; 80:7356–7363 [View Article] [PubMed]
    [Google Scholar]
  71. Wang H, Funchain P, Bebek G, Altemus J, Zhang H et al. Microbiomic differences in tumor and paired-normal tissue in head and neck squamous cell carcinomas. Genome Med 2017; 9:14 [View Article] [PubMed]
    [Google Scholar]
  72. Pushalkar S, Ji X, Li Y, Estilo C, Yegnanarayana R et al. Comparison of oral microbiota in tumor and non-tumor tissues of patients with oral squamous cell carcinoma. BMC Microbiol 2012; 12:144 [View Article] [PubMed]
    [Google Scholar]
  73. Eren AM, Borisy GG, Huse SM, Mark Welch JL. Oligotyping analysis of the human oral microbiome. Proc Natl Acad Sci U S A 2014; 111:E2875–84 [View Article] [PubMed]
    [Google Scholar]
  74. Mark Welch JL, Rossetti BJ, Rieken CW, Dewhirst FE, Borisy GG. Biogeography of a human oral microbiome at the micron scale. Proc Natl Acad Sci U S A 2016; 113:E791–800 [View Article] [PubMed]
    [Google Scholar]
  75. Shao W, Fujiwara N, Mouri Y, Kisoda S, Yoshida K et al. Conversion from epithelial to partial-EMT phenotype by Fusobacterium nucleatum infection promotes invasion of oral cancer cells. Sci Rep 2021; 11:14943 [View Article] [PubMed]
    [Google Scholar]
  76. Chen G, Gao C, Jiang S, Cai Q, Li R et al. Fusobacterium nucleatum outer membrane vesicles activate autophagy to promote oral cancer metastasis. J Adv Res 2023S2090-1232(23)00094-2 [View Article] [PubMed]
    [Google Scholar]
  77. Geng F, Zhang Y, Lu Z, Zhang S, Pan Y. Fusobacterium nucleatum caused DNA damage and promoted cell proliferation by the Ku70/P53 pathway in oral cancer cells. DNA Cell Biol 2020; 39:144–151
    [Google Scholar]
  78. Baty JJ, Stoner SN, Scoffield JA. Oral commensal streptococci: gatekeepers of the oral cavity. J Bacteriol 2022; 204:e0025722 [View Article] [PubMed]
    [Google Scholar]
  79. Tsai MS, Chen YY, Chen WC, Chen MF. Streptococcus mutans promotes tumor progression in oral squamous cell carcinoma. J Cancer 2022; 13:3358–3367 [View Article] [PubMed]
    [Google Scholar]
  80. Baraniya D, Jain V, Lucarelli R, Tam V, Vanderveer L et al. Screening of health-associated oral bacteria for anticancer properties in vitro. Front Cell Infect Microbiol 2020; 10:575656 [View Article] [PubMed]
    [Google Scholar]
  81. Xu Y, Jia Y, Chen L, Gao J, Yang D. Effect of Streptococcus anginosus on biological response of tongue squamous cell carcinoma cells. BMC Oral Health 2021; 21:141 [View Article] [PubMed]
    [Google Scholar]
  82. Baraniya D, Chitrala KN, Al-Hebshi NN. Global transcriptional response of oral squamous cell carcinoma cell lines to health-associated oral bacteria - an in vitro study. J Oral Microbiol 2022; 14:2073866 [View Article] [PubMed]
    [Google Scholar]
  83. Wang J, Sun F, Lin X, Li Z, Mao X et al. Cytotoxic T cell responses to Streptococcus are associated with improved prognosis of oral squamous cell carcinoma. Exp Cell Res 2018; 362:203–208 [View Article] [PubMed]
    [Google Scholar]
  84. Curry KD, Wang Q, Nute MG, Tyshaieva A, Reeves E et al. Emu: species-level microbial community profiling of full-length 16S rRNA Oxford Nanopore sequencing data. Nat Methods 2022; 19:845–853 [View Article] [PubMed]
    [Google Scholar]
  85. Johnson JS, Spakowicz DJ, Hong B-Y, Petersen LM, Demkowicz P et al. Evaluation of 16S rRNA gene sequencing for species and strain-level microbiome analysis. Nat Commun 2019; 10:5029 [View Article] [PubMed]
    [Google Scholar]
  86. Gao X, Sanderson SM, Dai Z, Reid MA, Cooper DE et al. Dietary methionine influences therapy in mouse cancer models and alters human metabolism. Nature 2019; 572:397–401 [View Article] [PubMed]
    [Google Scholar]
  87. Sedillo JC, Cryns VL. Targeting the methionine addiction of cancer. Am J Cancer Res 2022; 12:2249–2276 [PubMed]
    [Google Scholar]
  88. Pandit M, Kil Y-S, Ahn J-H, Pokhrel RH, Gu Y et al. Methionine consumption by cancer cells drives a progressive upregulation of PD-1 expression in CD4 T cells. Nat Commun 2023; 14:2593 [View Article] [PubMed]
    [Google Scholar]
  89. Bian Y, Li W, Kremer DM, Sajjakulnukit P, Li S et al. Cancer SLC43A2 alters T cell methionine metabolism and histone methylation. Nature 2020; 585:277–282 [View Article] [PubMed]
    [Google Scholar]
  90. Donohoe DR, Garge N, Zhang X, Sun W, O’Connell TM et al. The microbiome and butyrate regulate energy metabolism and autophagy in the mammalian colon. Cell Metab 2011; 13:517–526 [View Article] [PubMed]
    [Google Scholar]
  91. Comerford SA, Huang Z, Du X, Wang Y, Cai L et al. Acetate dependence of tumors. Cell 2014; 159:1591–1602 [View Article]
    [Google Scholar]
  92. Koh A, De Vadder F, Kovatcheva-Datchary P, Bäckhed F. From dietary fiber to host physiology: short-chain fatty acids as key bacterial metabolites. Cell 2016; 165:1332–1345 [View Article]
    [Google Scholar]
  93. van der Hee B, Wells JM. Microbial regulation of host physiology by short-chain fatty acids. Trends Microbiol 2021; 29:700–712 [View Article] [PubMed]
    [Google Scholar]
  94. Mima K, Sukawa Y, Nishihara R, Qian ZR, Yamauchi M et al. Fusobacterium nucleatum and T cells in colorectal carcinoma. JAMA Oncol 2015; 1:653–661 [View Article] [PubMed]
    [Google Scholar]
  95. Kosumi K, Baba Y, Yamamura K, Nomoto D, Okadome K et al. Intratumour Fusobacterium nucleatum and immune response to oesophageal cancer. Br J Cancer 2023; 128:1155–1165 [View Article] [PubMed]
    [Google Scholar]
  96. Dahlstrand Rudin A, Khamzeh A, Venkatakrishnan V, Basic A, Christenson K et al. Short chain fatty acids released by Fusobacterium nucleatum are neutrophil chemoattractants acting via free fatty acid receptor 2 (FFAR2). Cell Microbiol 2021; 23:e13348 [View Article] [PubMed]
    [Google Scholar]
  97. Mendes RT, Nguyen D, Stephens D, Pamuk F, Fernandes D et al. Endothelial cell response to Fusobacterium nucleatum. Infect Immun 2016; 84:2141–2148 [View Article] [PubMed]
    [Google Scholar]
  98. Wright HJ, Chapple ILC, Matthews JB, Cooper PR. Fusobacterium nucleatum regulation of neutrophil transcription. J Periodontal Res 2011; 46:1–12 [View Article] [PubMed]
    [Google Scholar]
  99. Neuzillet C, Marchais M, Vacher S, Hilmi M, Schnitzler A et al. Prognostic value of intratumoral Fusobacterium nucleatum and association with immune-related gene expression in oral squamous cell carcinoma patients. Sci Rep 2021; 11:7870 [View Article] [PubMed]
    [Google Scholar]
  100. Chan JYK, Cheung MK, Lan L, Ng C, Lau EHL et al. Characterization of oral microbiota in HPV and non-HPV head and neck squamous cell carcinoma and its association with patient outcomes. Oral Oncol 2022; 135:106245 [View Article] [PubMed]
    [Google Scholar]
  101. Mima K, Nishihara R, Qian ZR, Cao Y, Sukawa Y et al. Fusobacterium nucleatum in colorectal carcinoma tissue and patient prognosis. Gut 2016; 65:1973–1980 [View Article] [PubMed]
    [Google Scholar]
  102. Lehr K, Nikitina D, Vilchez-Vargas R, Steponaitiene R, Thon C et al. Microbial composition of tumorous and adjacent gastric tissue is associated with prognosis of gastric cancer. Sci Rep 2023; 13:4640 [View Article]
    [Google Scholar]
  103. Hsieh YY, Kuo WL, Hsu WT, Tung SY, Li C. Fusobacterium nucleatum-induced tumor mutation burden predicts poor survival of gastric cancer patients. Cancers 2022; 15:269 [View Article]
    [Google Scholar]
  104. Zhang N, Liu Y, Yang H, Liang M, Wang X et al. Clinical significance of Fusobacterium nucleatum infection and regulatory T cell enrichment in esophageal squamous cell carcinoma. Pathol Oncol Res 2021; 27:1609846 [View Article] [PubMed]
    [Google Scholar]
  105. Kataoka H, Taniguchi M, Fukamachi H, Arimoto T, Morisaki H et al. Rothia dentocariosa induces TNF-alpha production in a TLR2-dependent manner. Pathog Dis 2014; 71:65–68 [View Article] [PubMed]
    [Google Scholar]
  106. Maarsingh JD, Łaniewski P, Herbst-Kralovetz MM. Immunometabolic and potential tumor-promoting changes in 3D cervical cell models infected with bacterial vaginosis-associated bacteria. Commun Biol 2022; 5:725 [View Article] [PubMed]
    [Google Scholar]
  107. Altonsy MO, Andrews SC, Tuohy KM. Differential induction of apoptosis in human colonic carcinoma cells (Caco-2) by Atopobium, and commensal, probiotic and enteropathogenic bacteria: mediation by the mitochondrial pathway. Int J Food Microbiol 2010; 137:190–203 [View Article] [PubMed]
    [Google Scholar]
  108. Xu Z, Lv Z, Chen F, Zhang Y, Xu Z et al. Dysbiosis of human tumor microbiome and aberrant residence of Actinomyces in tumor-associated fibroblasts in young-onset colorectal cancer. Front Immunol 2022; 13: [View Article]
    [Google Scholar]
  109. Galeano Niño JL, Wu H, LaCourse KD, Kempchinsky AG, Baryiames A et al. Effect of the intratumoral microbiota on spatial and cellular heterogeneity in cancer. Nature 2022; 611:810–817 [View Article] [PubMed]
    [Google Scholar]
/content/journal/jmm/10.1099/jmm.0.001799
Loading
/content/journal/jmm/10.1099/jmm.0.001799
Loading

Data & Media loading...

Supplements

Supplementary material 1

PDF

Supplementary material 2

EXCEL
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error