1887

Abstract

The growing interest in microbiota–epigenetics–immune system research stems from the understanding that microbiota, a group of micro-organisms colonized in the human body, can influence the gene expression through epigenetic mechanisms and interaction with the immune system. Epigenetics refers to changes in gene activity that are not caused by the alteration in the DNA sequence itself.

The clinical significance of this research lies in the potential to develop new therapies for diseases linked to the imbalance of these microbial species (dysbiosis), such as cancer and neurodegenerative diseases. The intricate interaction between microbiota and epigenetics involves the production of metabolites and signalling molecules that can impact our health by influencing immune responses, metabolism and inflammation. Understanding these interactions could lead to novel therapeutic strategies targeting microbiota–epigenetic pathways to improve health outcomes.

In this context, we aim to review and emphasize the current knowledge and key concepts that link the microbiota to epigenetics and immune system function, exploring their relevance to the development and maintenance of homeostasis and susceptibility to different diseases later in life. We aim to elucidate key concepts concerning the interactions and potential effects among the human gut microbiota, epigenetics, the immune system and ageing diseases linked to dysbiosis.

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2024-11-28
2024-12-08
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References

  1. Woo V, Alenghat T. Epigenetic regulation by gut microbiota. Gut Microbes 2022; 14:2022407 [View Article] [PubMed]
    [Google Scholar]
  2. Allen J, Hao S, Sears CL, Timp W. Epigenetic changes induced by Bacteroides fragilis toxin. Infect Immun 2019; 87:e00447–18 [View Article]
    [Google Scholar]
  3. Erny D, Dokalis N, Mezö C, Castoldi A, Mossad O et al. Microbiota-derived acetate enables the metabolic fitness of the brain innate immune system during health and disease. Cell Metab 2021; 33:2260–2276 [View Article] [PubMed]
    [Google Scholar]
  4. Miro-Blanch J, Yanes O. Epigenetic regulation at the interplay between gut microbiota and host metabolism. Front Genet 2019; 10:638 [View Article] [PubMed]
    [Google Scholar]
  5. Tirthani E, Said MS, Rehman A. Genetics and obesity. In StatPearls Treasure Island (FL): StatPearls Publishing; 2021
    [Google Scholar]
  6. Gupta N, El-Gawaad NSA, Mallasiy LO, Gupta H, Yadav VK. Microbial dysbiosis and the aging process: a review on the potential age-deceleration role of Lactiplantibacillus plantarum. Front Microbiol 2024; 15:1260793 [View Article] [PubMed]
    [Google Scholar]
  7. Hullar MAJ, Fu BC. Diet, the gut microbiome, and epigenetics. Cancer J 2014; 20:170–175 [View Article] [PubMed]
    [Google Scholar]
  8. Wang B, Yao M, Lv L, Ling Z, Li L. The human microbiota in health and disease. Engineering 2017; 3:71–82 [View Article]
    [Google Scholar]
  9. Zheng D, Liwinski T, Elinav E. Interaction between microbiota and immunity in health and disease. Cell Res 2020; 30:492–506 [View Article] [PubMed]
    [Google Scholar]
  10. Conrad R, Vlassov AV. The human microbiota: composition, functions, and therapeutic potential. Med Sci Monit 2015; 2:92–103
    [Google Scholar]
  11. Gilbert JA, Blaser MJ, Caporaso JG, Jansson JK, Lynch SV et al. Current understanding of the human microbiome. Nat Med 2018; 24:392–400 [View Article] [PubMed]
    [Google Scholar]
  12. Mangiola F, Nicoletti A, Gasbarrini A, Ponziani FR. Gut microbiota and aging. Eur Rev Med Pharmacol Sci 2018; 22:7404–7413 [View Article] [PubMed]
    [Google Scholar]
  13. Kaur H, Singh Y, Singh S, Singh RB. Gut microbiome-mediated epigenetic regulation of brain disorder and application of machine learning for multi-omics data analysis. Genome 2021; 64:355–371 [View Article] [PubMed]
    [Google Scholar]
  14. Ursell LK, Metcalf JL, Parfrey LW, Knight R. Defining the human microbiome. Nutr Rev 2012; 70 Suppl 1:S38–44 [View Article] [PubMed]
    [Google Scholar]
  15. Rinninella E, Raoul P, Cintoni M, Franceschi F, Miggiano GAD et al. What is the healthy gut microbiota composition? A changing ecosystem across age, environment, diet, and diseases. Microorganisms 2019; 7:14 [View Article] [PubMed]
    [Google Scholar]
  16. Cotillard A, Kennedy SP, Kong LC, Prifti E, Pons N et al. Dietary intervention impact on gut microbial gene richness. Nature 2013; 500:585–588 [View Article] [PubMed]
    [Google Scholar]
  17. Bokulich NA, Chung J, Battaglia T, Henderson N, Jay M. Antibiotics, birth mode, and diet shape microbiome maturation during early life. Sci Transl Med 2016; 8:343ra82 [View Article]
    [Google Scholar]
  18. Sharma S, Tripathi P. Gut microbiome and type 2 diabetes: where we are and where to go?. J Nutr Biochem 2019; 63:101–108 [View Article]
    [Google Scholar]
  19. Dominguez-Bello MG, Costello EK, Contreras M, Magris M, Hidalgo G et al. Delivery mode shapes the acquisition and structure of the initial microbiota across multiple body habitats in newborns. Proc Natl Acad Sci USA 2010; 107:11971–11975 [View Article]
    [Google Scholar]
  20. Paul B, Barnes S, Demark-Wahnefried W, Morrow C, Salvador C et al. Influences of diet and the gut microbiome on epigenetic modulation in cancer and other diseases. Clin Epigenet 2015; 7:1–11 [View Article]
    [Google Scholar]
  21. Valdes AM, Walter J, Segal E, Spector TD. Role of the gut microbiota in nutrition and health. BMJ 2018; 361:k2179 [View Article] [PubMed]
    [Google Scholar]
  22. Loftus M, Hassouneh SA-D, Yooseph S. Bacterial associations in the healthy human gut microbiome across populations. Sci Rep 2021; 11:2828 [View Article] [PubMed]
    [Google Scholar]
  23. Thursby E, Juge N. Introduction to the human gut microbiota. Biochem J 2017; 474:1823–1836 [View Article] [PubMed]
    [Google Scholar]
  24. Wen L, Duffy A. Factors influencing the gut microbiota, inflammation, and type 2 diabetes. J Nutr 2017; 147:1468S–1475S [View Article] [PubMed]
    [Google Scholar]
  25. Qin Y, Wade PA. Crosstalk between the microbiome and epigenome: messages from bugs. J Biochem 2018; 163:105–112 [View Article] [PubMed]
    [Google Scholar]
  26. Nikolaieva N, Sevcikova A, Omelka R, Martiniakova M, Mego M et al. Gut microbiota–MicroRNA interactions in intestinal homeostasis and cancer development. Microorganisms 2023; 11:107 [View Article]
    [Google Scholar]
  27. de Sire A, de Sire R, Petito V, Masi L, Cisari C et al. Gut-joint axis: the role of physical exercise on gut microbiota modulation in older people with osteoarthritis. Nutrients 2020; 12:574 [View Article] [PubMed]
    [Google Scholar]
  28. Nikolaieva N, Sevcikova A, Omelka R, Martiniakova M, Mego M et al. Gut microbiota-MicroRNA interactions in intestinal homeostasis and cancer development. Microorganisms 2022; 11:107 [View Article] [PubMed]
    [Google Scholar]
  29. Miller KD, Schug ZT. Targeting acetate metabolism: achilles’ nightmare. Br J Cancer 2021; 124:1900–1901
    [Google Scholar]
  30. Prasher D, Greenway SC, Singh RB. The impact of epigenetics on cardiovascular disease. Biochem Cell Biol 2020; 98:12–22 [View Article] [PubMed]
    [Google Scholar]
  31. Cavalli G, Heard E. Advances in epigenetics link genetics to the environment and disease. Nature 2019; 571:489–499
    [Google Scholar]
  32. Dempsey J, Zhang A, Cui JY. Coordinate regulation of long non-coding RNAs and protein-coding genes in germ-free mice. BMC Genom 2018; 19:834 [View Article] [PubMed]
    [Google Scholar]
  33. Devaux CA, Raoult D. The microbiological memory, an epigenetic regulator governing the balance between good health and metabolic disorders. Front Microbiol 2018; 9:1379 [View Article] [PubMed]
    [Google Scholar]
  34. Anastasiadou E, Jacob LS, Slack FJ. Non-coding RNA networks in cancer. Nat Rev Cancer 2018; 18:5–18 [View Article] [PubMed]
    [Google Scholar]
  35. Gomes AQ, Nolasco S, Soares H. Non-coding RNAs: multi-tasking molecules in the cell. Int J Mol Sci 2013; 14:16010–16039 [View Article] [PubMed]
    [Google Scholar]
  36. Li E, Zhang Y. DNA methylation in mammals. Cold Spring Harb Perspect Biol 2014; 6:a019133 [View Article] [PubMed]
    [Google Scholar]
  37. Sadakierska-Chudy A, Filip M. A comprehensive view of the epigenetic landscape. Part II: histone post-translational modification, nucleosome level, and chromatin regulation by ncRNAs. Neurotox Res 2015; 27:172–197 [View Article] [PubMed]
    [Google Scholar]
  38. Cruvinel W, Mesquita Júnior D, Araújo JAP, Catelan TTT, Souza A et al. Immune system: Part I. Fundamentals of innate immunity with emphasis on molecular and cellular mechanisms of inflammatory response. Rev Bras Reumatol Engl Ed 2010; 50:434–447
    [Google Scholar]
  39. Bulut O, Kilic G, Domínguez-Andrés J, Netea MG. Overcoming immune dysfunction in the elderly: trained immunity as a novel approach. Int Immunol 2020; 32:741–753 [View Article] [PubMed]
    [Google Scholar]
  40. Brauning A, Rae M, Zhu G, Fulton E, Admasu TD et al. Aging of the immune system: focus on natural killer cells phenotype and functions. Cells 2022; 11:1017 [View Article] [PubMed]
    [Google Scholar]
  41. Kim YJ, Kim BK, Park SJ, Kim JH. Impact of Fusobacterium nucleatum in the gastrointestinal tract on natural killer cells. World J Gastroenterol 2021; 27:4879–4889 [View Article] [PubMed]
    [Google Scholar]
  42. Ben-Shmuel A, Sabag B, Biber G, Barda-Saad M. The role of the cytoskeleton in regulating the natural killer cell immune response in health and disease: from signaling dynamics to function. Front Cell Dev Biol 2021; 9:609532 [View Article] [PubMed]
    [Google Scholar]
  43. Ning Z, Liu Y, Guo D, Lin W-J, Tang Y. Natural killer cells in the central nervous system. Cell Commun Signal 2023; 21:341 [View Article] [PubMed]
    [Google Scholar]
  44. Wiedemann GM. Localization matters: epigenetic regulation of natural killer cells in different tissue microenvironments. Front Immunol 2022; 13:913054 [View Article]
    [Google Scholar]
  45. Hsiao WWL, Metz C, Singh DP, Roth J. The microbes of the intestine: an introduction to their metabolic and signaling capabilities. Endocrinol Metab Clin North Am 2008; 37:857–871 [View Article] [PubMed]
    [Google Scholar]
  46. Messer JS, Liechty ER, Vogel OA, Chang EB. Evolutionary and ecological forces that shape the bacterial communities of the human gut. Mucosal Immunol 2017; 10:567–579 [View Article] [PubMed]
    [Google Scholar]
  47. Zhang Y, Parajuli KR, Fava GE, Gupta R, Xu W et al. GLP-1 receptor in pancreatic α-cells regulates glucagon secretion in a glucose-dependent bidirectional manner. Diabetes 2019; 68:34–44 [View Article]
    [Google Scholar]
  48. Yamane S, Inagaki N. Regulation of glucagon‐like peptide‐1 sensitivity by gut microbiota dysbiosis. J Diabetes Invest 2018; 9:262–264 [View Article]
    [Google Scholar]
  49. Hou K, Wu Z-X, Chen X-Y, Wang J-Q, Zhang D et al. Microbiota in health and diseases. Signal Transduct Target Ther 2022; 7:135 [View Article] [PubMed]
    [Google Scholar]
  50. Al Bander Z, Nitert MD, Mousa A, Naderpoor N. The gut microbiota and inflammation: an overview. Int J Environ Res Public Health 2020; 17:7618 [View Article] [PubMed]
    [Google Scholar]
  51. Baker JM, Al-Nakkash L, Herbst-Kralovetz MM. Estrogen–gut microbiome axis: physiological and clinical implications. Maturitas 2017; 103:45–53
    [Google Scholar]
  52. Yuille S, Reichardt N, Panda S, Dunbar H, Mulder IE et al. Human gut bacteria as potent class I histone deacetylase inhibitors in vitro through production of butyric acid and valeric acid. PloS one 2018; 13:e0201073
    [Google Scholar]
  53. Ruusunen A, Rocks T, Jacka F, Loughman A. The gut microbiome in anorexia nervosa: relevance for nutritional rehabilitation. Psychopharmacology 2019; 236:1545–1558 [View Article] [PubMed]
    [Google Scholar]
  54. Sharma M, Li Y, Stoll ML, Tollefsbol TO. The epigenetic connection between the gut microbiome in obesity and diabetes. Front Genet 2019; 10:1329 [View Article] [PubMed]
    [Google Scholar]
  55. El-Sayed A, Aleya L, Kamel M. Microbiota and epigenetics: promising therapeutic approaches?. Environ Sci Pollut Res Int 2021; 28:49343–49361 [View Article] [PubMed]
    [Google Scholar]
  56. Takahashi D, Hase K. Commensal microbiota-derived signals regulate host immune system through epigenetic modifications. Inflam Regener 2015; 35:129–136 [View Article]
    [Google Scholar]
  57. Yoo JY, Groer M, Dutra SVO, Sarkar A, McSkimming DI. Gut microbiota and immune system interactions. Microorganisms 2020; 8:1587 [View Article] [PubMed]
    [Google Scholar]
  58. Belkaid Y, Hand TW. Role of the microbiota in immunity and inflammation. Cell 2014; 157:121–141 [View Article] [PubMed]
    [Google Scholar]
  59. Ragonnaud E, Biragyn A. Gut microbiota as the key controllers of “healthy” aging of elderly people. Immun Ageing 2021; 18:2 [View Article] [PubMed]
    [Google Scholar]
  60. Nagpal R, Mainali R, Ahmadi S, Wang S, Singh R et al. Gut microbiome and aging: physiological and mechanistic insights. Nutr Healthy Aging 2018; 4:267–285 [View Article] [PubMed]
    [Google Scholar]
  61. Soderholm AT, Pedicord VA. Intestinal epithelial cells: at the interface of the microbiota and mucosal immunity. Immunology 2019; 158:267–280 [View Article] [PubMed]
    [Google Scholar]
  62. Ali A, Tan H, Kaiko GE. Role of the intestinal epithelium and its interaction with the microbiota in food allergy. Front Immunol 2020; 11:3222 [View Article]
    [Google Scholar]
  63. Janssen AWF, Houben T, Katiraei S, Dijk W, Boutens L et al. Modulation of the gut microbiota impacts nonalcoholic fatty liver disease: a potential role for bile acids. J Lipid Res 2017; 58:1399–1416 [View Article] [PubMed]
    [Google Scholar]
  64. Allin KH, Nielsen T, Pedersen O. Mechanisms in endocrinology: gut microbiota in patients with type 2 diabetes mellitus. Eur J Endocrinol 2015; 172:R167–77 [View Article] [PubMed]
    [Google Scholar]
  65. Ley RE, Turnbaugh PJ, Klein S, Gordon JI. Human gut microbes associated with obesity. Nature 2006; 444:1022–1023 [View Article]
    [Google Scholar]
  66. Rodríguez-Rodero S, Fernández-Morera JL, Menéndez-Torre E, Calvanese V, Fernández AF et al. Aging genetics and aging. Aging Dis 2011; 2:186–195 [PubMed]
    [Google Scholar]
  67. Khan SS, Singer BD, Vaughan DE. Molecular and physiological manifestations and measurement of aging in humans. Aging Cell 2017; 16:624–633 [View Article]
    [Google Scholar]
  68. Lian J, Yue Y, Yu W, Zhang Y. Immunosenescence: a key player in cancer development. J Hematol Oncol 2020; 13:1–18 [View Article]
    [Google Scholar]
  69. Franceschi C, Garagnani P, Parini P, Giuliani C, Santoro A. Inflammaging: a new immune–metabolic viewpoint for age-related diseases. Nat Rev Endocrinol 2018; 14:576–590 [View Article]
    [Google Scholar]
  70. Odamaki T, Kato K, Sugahara H, Hashikura N, Takahashi S et al. Age-related changes in gut microbiota composition from newborn to centenarian: a cross-sectional study. BMC Microbiol 2016; 16:1–12 [View Article]
    [Google Scholar]
  71. Salazar N, Valdés-Varela L, González S, Gueimonde M, de Los Reyes-Gavilán CG. Nutrition and the gut microbiome in the elderly. Gut Microbes 2017; 8:82–97 [View Article] [PubMed]
    [Google Scholar]
  72. Popkes M, Valenzano DR. Microbiota–host interactions shape ageing dynamics. Phil Trans R Soc B 2020; 375:20190596 [View Article]
    [Google Scholar]
  73. Aleman FDD, Valenzano DR. Microbiome evolution during host aging. PLoS Pathog 2019; 15:e1007727 [View Article]
    [Google Scholar]
  74. Wei Z-Y, Rao J-H, Tang M-T, Zhao G-A, Li Q-C et al. Characterization of dynamic age-dependent changes and driver microbes in primate gut microbiota during host’s development and healthy aging via captive crab-eating macaque model. Microbiology 2020 [View Article]
    [Google Scholar]
  75. Gadecka A, Bielak-Zmijewska A. Slowing down ageing: the role of nutrients and microbiota in modulation of the epigenome. Nutrients 2019; 11:1251 [View Article] [PubMed]
    [Google Scholar]
  76. Sereme Y, Mezouar S, Grine G, Mege JL, Drancourt M et al. Methanogenic archaea: emerging partners in the field of allergic diseases. Clinic Rev Allerg Immunol 2019; 57:456–466 [View Article]
    [Google Scholar]
  77. Mayer F, Müller V. Adaptations of anaerobic archaea to life under extreme energy limitation. FEMS Microbiol Rev 2014; 38:449–472 [View Article] [PubMed]
    [Google Scholar]
  78. Ishaq SL, Moses PL, Wright A-D. The pathology of methanogenic archaea in human gastrointestinal tract disease. Gut Microbiome Implic Hum Dis 2016 [View Article]
    [Google Scholar]
  79. Sedley L. Advances in nutritional epigenetics—a fresh perspective for an old idea. lessons learned, limitations, and future directions. Epigenet Insights 2020; 13:2516865720981924
    [Google Scholar]
  80. Maczulak AE, Wolin MJ, Miller TL. Increase in colonic methanogens and total anaerobes in aging rats. Appl Environ Microbiol 1989; 55:2468–2473 [View Article] [PubMed]
    [Google Scholar]
  81. Maynard C, Weinkove D. The gut microbiota and ageing. In Biochemistry and Cell Biology of Ageing: Part I Biomedical Science 2018 pp 351–371 [View Article]
    [Google Scholar]
  82. von Frieling J, Fink C, Hamm J, Klischies K, Forster M et al. Grow with the challenge - microbial effects on epithelial proliferation, carcinogenesis, and cancer therapy. Front Microbiol 2018; 9:2020 [View Article] [PubMed]
    [Google Scholar]
  83. Fila M, Chojnacki C, Chojnacki J, Blasiak J. Is an “epigenetic diet” for migraines justified? The case of folate and DNA methylation. Nutrients 2019; 11:2763 [View Article] [PubMed]
    [Google Scholar]
  84. Singh S, Sharma P, Sarma D, Kumawat M, Tiwari R et al. Implication of obesity and gut microbiome dysbiosis in the etiology of colorectal cancer. Cancers 2023; 15:1913 [View Article]
    [Google Scholar]
  85. Dayeh T, Volkov P, Salö S, Hall E, Nilsson E et al. Genome-wide DNA methylation analysis of human pancreatic islets from type 2 diabetic and non-diabetic donors identifies candidate genes that influence insulin secretion. PLoS Genet 2014; 10:e1004160 [View Article]
    [Google Scholar]
  86. Dávalos A, Goedeke L, Smibert P, Ramírez CM, Warrier NP et al. miR-33a/b contribute to the regulation of fatty acid metabolism and insulin signaling. Proc Natl Acad Sci USA 2011; 108:9232–9237 [View Article]
    [Google Scholar]
  87. Trajkovski M, Hausser J, Soutschek J, Bhat B, Akin A et al. MicroRNAs 103 and 107 regulate insulin sensitivity. Nature 2011; 474:649–653 [View Article] [PubMed]
    [Google Scholar]
  88. Chiefari E, Mirabelli M, La Vignera S, Tanyolaç S, Foti DP et al. Insulin resistance and cancer: in search for a causal link. Int J Mol Sci 2021; 22:11137 [View Article] [PubMed]
    [Google Scholar]
  89. Lee S-H, Park S-Y, Choi CS. Insulin resistance: from mechanisms to therapeutic strategies. Diabetes Metab J 2022; 46:15–37 [View Article] [PubMed]
    [Google Scholar]
  90. Lega IC, Lipscombe LL. Review: diabetes, obesity, and cancer—pathophysiology and clinical implications. Endocr Rev 2020; 41:33–52 [View Article]
    [Google Scholar]
  91. Ahmad Kendong SM, Raja Ali RA, Nawawi KNM, Ahmad HF, Mokhtar NM. Gut dysbiosis and intestinal barrier dysfunction: potential explanation for early-onset colorectal cancer. Front Cell Infect Microbiol 2021; 11:744606 [View Article] [PubMed]
    [Google Scholar]
  92. Allegra A, Musolino C, Tonacci A, Pioggia G, Gangemi S. Interactions between the MicroRNAs and microbiota in cancer development: roles and therapeutic opportunities. Cancers 2020; 12:805 [View Article] [PubMed]
    [Google Scholar]
  93. Ye J, Wu W, Li Y, Li L. Influences of the gut microbiota on DNA methylation and histone modification. Dig Dis Sci 2017; 62:1155–1164 [View Article]
    [Google Scholar]
  94. Sarkar S, Abujamra AL, Loew JE, Forman LW, Perrine SP et al. Histone deacetylase inhibitors reverse CpG methylation by regulating DNMT1 through ERK signaling. Anticancer Res 2011; 31:2723–2732 [PubMed]
    [Google Scholar]
  95. Zhao K, Hu Y. Microbiome harbored within tumors: a new chance to revisit our understanding of cancer pathogenesis and treatment. Sig Transduct Target Ther 2020; 5:136 [View Article]
    [Google Scholar]
  96. Zhao L-Y, Mei J-X, Yu G, Lei L, Zhang W-H et al. Role of the gut microbiota in anticancer therapy: from molecular mechanisms to clinical applications. Sig Transduct Target Ther 2023; 8:201 [View Article]
    [Google Scholar]
  97. Kamada N, Seo SU, Chen GY, Núñez G. Role of the gut microbiota in immunity and inflammatory disease. Nat Rev Immunol 2013; 13:321–335
    [Google Scholar]
  98. Nicholson JK, Holmes E, Kinross J, Burcelin R, Gibson G et al. Host-gut microbiota metabolic interactions. Science 2012; 336:1262–1267 [View Article]
    [Google Scholar]
  99. Romano KA, Vivas EI, Amador-Noguez D, Rey FE. Intestinal microbiota composition modulates choline bioavailability from diet and accumulation of the proatherogenic metabolite trimethylamine- N -oxide. mBio 2015; 6:e02481–14 [View Article]
    [Google Scholar]
  100. Fennema D, Phillips IR, Shephard EA. Trimethylamine and trimethylamine N-oxide, a flavin-containing monooxygenase 3 (FMO3)-mediated host-microbiome metabolic axis implicated in health and disease. Drug Metab Dispos 2016; 44:1839–1850 [View Article]
    [Google Scholar]
  101. Velasquez MT, Ramezani A, Manal A, Raj DS. Trimethylamine N-oxide: the good, the bad and the unknown. Toxins 2016; 8:326 [View Article] [PubMed]
    [Google Scholar]
  102. Tang WHW, Hazen SL. Microbiome, trimethylamine N-oxide, and cardiometabolic disease. Translatl Res 2017; 179:108–115 [View Article]
    [Google Scholar]
  103. Ruan G, Chen M, Chen L, Xu F, Xiao Z et al. Roseburia intestinalis and its metabolite butyrate inhibit colitis and upregulate TLR5 through the SP3 signaling pathway. Nutrients 2022; 14:3041 [View Article]
    [Google Scholar]
  104. Ortega Avila JG, Echeverri I, de Plata CA, Castillo A. Impact of oxidative stress during pregnancy on fetal epigenetic patterns and early origin of vascular diseases. Nutr Rev 2015; 73:12–21 [View Article]
    [Google Scholar]
  105. Vezza T, Abad-Jiménez Z, Marti-Cabrera M, Rocha M, Víctor VM. Microbiota-mitochondria inter-talk: a potential therapeutic strategy in obesity and type 2 diabetes. Antioxidants 2020; 9:848 [View Article]
    [Google Scholar]
  106. Stols-Gonçalves D, Tristão LS, Henneman P, Nieuwdorp M. Epigenetic markers and microbiota/metabolite-induced epigenetic modifications in the pathogenesis of obesity, metabolic syndrome, type 2 diabetes, and non-alcoholic fatty liver disease. Curr Diab Rep 2019; 19:31 [View Article] [PubMed]
    [Google Scholar]
  107. Li M, Chen W-D, Wang Y-D. The roles of the gut microbiota–miRNA interaction in the host pathophysiology. Mol Med 2020; 26:1–9 [View Article]
    [Google Scholar]
  108. Carabotti M, Scirocco A, Maselli MA, Severi C. The gut-brain axis: interactions between enteric microbiota, central and enteric nervous systems. Annal Gastroenterol 2015; 28:203
    [Google Scholar]
  109. de la Fuente-Nunez C, Meneguetti BT, Franco OL, Lu TK. Neuromicrobiology: how microbes influence the brain. ACS Chem Neurosci 2018; 9:141–150 [View Article]
    [Google Scholar]
  110. Ghosh TS, Shanahan F, O’Toole PW. The gut microbiome as a modulator of healthy ageing. Nat Rev Gastroenterol Hepatol 2022; 19:565–584 [View Article] [PubMed]
    [Google Scholar]
  111. Tiwari P, Dwivedi R, Bansal M, Tripathi M, Dada R. Role of gut microbiota in neurological disorders and its therapeutic significance. J Clin Med 2023; 12:1650 [View Article] [PubMed]
    [Google Scholar]
  112. Zhu X, Li B, Lou P, Dai T, Chen Y et al. The relationship between the gut microbiome and neurodegenerative diseases. Neurosci Bull 2021; 37:1510–1522 [View Article] [PubMed]
    [Google Scholar]
  113. Cryan JF, O’Mahony SM. The microbiome-gut-brain axis: from bowel to behavior. Neurogastroenterol Motility 2011; 23:187–192 [View Article]
    [Google Scholar]
  114. Yang B, Wei J, Ju P, Chen J. Effects of regulating intestinal microbiota on anxiety symptoms: a systematic review. Gen Psychiatr 2019; 32:e100056 [View Article] [PubMed]
    [Google Scholar]
  115. Carrard A, Elsayed M, Margineanu M, Boury-Jamot B, Fragnière L et al. Peripheral administration of lactate produces antidepressant-like effects. Mol Psychiatry 2018; 23:392–399 [View Article] [PubMed]
    [Google Scholar]
  116. Karnib N, El-Ghandour R, El Hayek L, Nasrallah P, Khalifeh M et al. Lactate is an antidepressant that mediates resilience to stress by modulating the hippocampal levels and activity of histone deacetylases. Neuropsychopharmacology 2019; 44:1152–1162 [View Article] [PubMed]
    [Google Scholar]
  117. You X-Y, Zhang H-Y, Han X, Wang F, Zhuang P-W et al. Intestinal mucosal barrier is regulated by intestinal tract neuro-immune interplay. Front Pharmacol 2021; 12:659716 [View Article] [PubMed]
    [Google Scholar]
  118. Cryan JF, O’Riordan KJ, Cowan CSM, Sandhu KV, Bastiaanssen TFS et al. The microbiota-gut-brain axis. Physiol Rev 2019; 99:1877–2013 [View Article]
    [Google Scholar]
  119. Tian S, Chen M. Global research progress of gut microbiota and epigenetics: bibliometrics and visualized analysis. Front Immunol 2024; 15:1412640 [View Article] [PubMed]
    [Google Scholar]
  120. Grezenko H, Ekhator C, Nwabugwu NU, Ganga H, Affaf M et al. Epigenetics in neurological and psychiatric disorders: a comprehensive review of current understanding and future perspectives. Cureus 2023; 15:e43960 [View Article] [PubMed]
    [Google Scholar]
  121. Tilocca B, Pieroni L, Soggiu A, Britti D, Bonizzi L et al. Gut–brain axis and neurodegeneration: state-of-the-art of meta-omics sciences for microbiota characterization. Int J Mol Sci 2020; 21:4045 [View Article]
    [Google Scholar]
  122. Xiao J, Wang T, Xu Y, Gu X, Li D et al. Long-term probiotic intervention mitigates memory dysfunction through a novel H3K27me3-based mechanism in lead-exposed rats. Transl Psychiatry 2020; 10:1–18 [View Article]
    [Google Scholar]
  123. Cani PD, Bibiloni R, Knauf C, Waget A, Neyrinck AM et al. Changes in gut microbiota control metabolic endotoxemia-induced inflammation in high-fat diet–induced obesity and diabetes in mice. Diabetes 2008; 57:1470–1481 [View Article]
    [Google Scholar]
  124. Lee CJ, Sears CL, Maruthur N. Gut microbiome and its role in obesity and insulin resistance. Ann N Y Acad Sci 2020; 1461:37–52 [View Article] [PubMed]
    [Google Scholar]
  125. Caricilli AM, Saad MJ. The role of gut microbiota on insulin resistance. Nutrients 2013; 5:829–851 [View Article]
    [Google Scholar]
  126. Berg G, Rybakova D, Fischer D, Cernava T, Vergès M-CC et al. Microbiome definition re-visited: old concepts and new challenges. Microbiome 2020; 8:103 [View Article] [PubMed]
    [Google Scholar]
  127. Huang J-T, Mao Y-Q, Han B, Zhang Z-Y, Chen H-L et al. Calorie restriction conferred improvement effect on long-term rehabilitation of ischemic stroke via gut microbiota. Pharmacol Res 2021; 170:105726 [View Article]
    [Google Scholar]
  128. Chen Y, Peng L, Shi S, Guo G, Wen H. Boeravinone B alleviates gut dysbiosis during myocardial infarction-induced cardiotoxicity in rats. J Cell Mol Med 2021; 25:6403–6416 [View Article] [PubMed]
    [Google Scholar]
  129. Barone M, Mendozzi L, D’Amico F, Saresella M, Rampelli S et al. Influence of a high-impact multidimensional rehabilitation program on the gut microbiota of patients with multiple sclerosis. Int J Mol Sci 2021; 22:7173 [View Article] [PubMed]
    [Google Scholar]
  130. Durack J, Lynch SV. The gut microbiome: relationships with disease and opportunities for therapy. J Exp Med 2019; 216:20–40 [View Article] [PubMed]
    [Google Scholar]
  131. Ahn J, Hayes RB. Environmental influences on the human microbiome and implications for noncommunicable disease. Annu Rev Public Health 2021; 42:277–292 [View Article]
    [Google Scholar]
  132. Christian VJ, Miller KR, Martindale RG. Food insecurity, malnutrition, and the microbiome. Curr Nutr Rep 2020; 9:356–360 [View Article] [PubMed]
    [Google Scholar]
  133. Casals-Pascual C, Vergara A, Vila J. Intestinal microbiota and antibiotic resistance: perspectives and solutions. Hum Microb J 2018; 9:11–15 [View Article]
    [Google Scholar]
  134. Napolitano M, Covasa M. Microbiota transplant in the treatment of obesity and diabetes: current and future perspectives. Front Microbiol 2020; 11:590370 [View Article] [PubMed]
    [Google Scholar]
  135. Heijtz RD, Gonzalez-Santana A, Laman JD. Young microbiota rejuvenates the aging brain. Nat Aging 2021; 1:625–627 [View Article]
    [Google Scholar]
  136. Lozupone M, D’Urso F, Piccininni C, Montagna ML, Sardone R et al. The relationship between epigenetics and microbiota in neuropsychiatric diseases. Epigenomics 2020; 12:1559–1568 [View Article]
    [Google Scholar]
  137. Sobhani I, Bergsten E, Couffin S, Amiot A, Nebbad B et al. Colorectal cancer-associated microbiota contributes to oncogenic epigenetic signatures. Proc Natl Acad Sci USA 2019; 116:24285–24295 [View Article] [PubMed]
    [Google Scholar]
  138. Heard E, Martienssen RA. Transgenerational epigenetic inheritance: myths and mechanisms. Cell 2014; 157:95–109 [View Article] [PubMed]
    [Google Scholar]
  139. Bartolini I, Risaliti M, Tucci R, Muiesan P, Ringressi MN et al. Gut microbiota and immune system in liver cancer: promising therapeutic implication from development to treatment. World J Gastrointest Oncol 2021; 13:1616–1631 [View Article] [PubMed]
    [Google Scholar]
  140. Salazar N, González S, Nogacka AM, Rios-Covián D, Arboleya S et al. Microbiome: effects of ageing and diet. Curr Issues Mol Biol 2020; 36:33–62 [View Article] [PubMed]
    [Google Scholar]
  141. Xu J, Xu H, Yang M, Liang Y, Peng Q et al. New insights into the epigenetic regulation of inflammatory bowel disease. Front Pharmacol 2022; 13:68 [View Article]
    [Google Scholar]
  142. De Silva S, Tennekoon KH, Karunanayake EH. Interaction of gut microbiome and host microRNAs with the occurrence of colorectal and breast cancer and their impact on patient immunity. Onco Targets Ther 2021; 14:5115–5129 [View Article] [PubMed]
    [Google Scholar]
  143. Zhao Y, Wang C, Goel A. Role of gut microbiota in epigenetic regulation of colorectal cancer. Biochimica et Biophysica Acta (BBA) - Rev Cancer 2021; 1875:188490 [View Article]
    [Google Scholar]
  144. Sun D, Chen Y, Fang J-Y. Influence of the microbiota on epigenetics in colorectal cancer. Natl Sci Rev 2019; 6:1138–1148 [View Article] [PubMed]
    [Google Scholar]
  145. Zhou Z, Chen J, Yao H, Hu H. Fusobacterium and colorectal cancer. Front Oncol 2018; 8:371 [View Article]
    [Google Scholar]
  146. De Bruyn F, Beauprez J, Maertens J, Soetaert W, De Mey M. Unraveling the Leloir pathway of Bifidobacterium bifidum: significance of the uridylyltransferases. Appl Environ Microbiol 2013; 79:7028–7035 [View Article] [PubMed]
    [Google Scholar]
  147. Badal VD, Vaccariello ED, Murray ER, Yu KE, Knight R et al. The gut microbiome, aging, and longevity: a systematic review. Nutrients 2020; 12:3759 [View Article] [PubMed]
    [Google Scholar]
  148. Lin T-L, Shu C-C, Chen Y-M, Lu J-J, Wu T-S et al. Like cures like: pharmacological activity of anti-inflammatory lipopolysaccharides from gut microbiome. Front Pharmacol 2020; 11:554 [View Article] [PubMed]
    [Google Scholar]
  149. Lee C-C, Chiu C-H. Link between gut microbiota and neonatal sepsis. J Formosan Med Assoc 2024; 123:638–646 [View Article] [PubMed]
    [Google Scholar]
  150. Booth J. Fusobacterium infections. In xPharm: The Comprehensive Pharmacology Reference Elsevier Inc; 2007 pp 1–3 [View Article]
    [Google Scholar]
  151. Kelly D, Yang L, Pei Z. Gut microbiota, fusobacteria, and colorectal cancer. Diseases 2018; 6:109
    [Google Scholar]
  152. Afra K, Laupland K, Leal J, Lloyd T, Gregson D. Incidence, risk factors, and outcomes of Fusobacterium species bacteremia. BMC Infect Dis 2013; 13:1–6 [View Article] [PubMed]
    [Google Scholar]
  153. Arane K, Goldman RD. Fusobacterium infections in children. Can Fam Physician 2016; 62:813–814 [PubMed]
    [Google Scholar]
  154. Donovan SM, Wang M, Li M, Friedberg I, Schwartz SL et al. Host-microbe interactions in the neonatal intestine: role of human milk oligosaccharides. Adv Nutr 2012; 3:450S–5S [View Article] [PubMed]
    [Google Scholar]
  155. Martinez E, Taminiau B, Rodriguez C, Daube G. Gut microbiota composition associated with Clostridioides difficile colonization and infection. Pathogens 2022; 11:781 [View Article] [PubMed]
    [Google Scholar]
  156. Kovatcheva-Datchary P, Arora T. Nutrition, the gut microbiome and the metabolic syndrome. Best Practice Res Clin Gastroenterol 2013; 27:59–72 [View Article]
    [Google Scholar]
  157. Mora-Janiszewska O, Faryniak-Zuzak A, Darmochwał-Kolarz D. Epigenetic links between microbiota and gestational diabetes. Int J Mol Sci 2022; 23:1831 [View Article] [PubMed]
    [Google Scholar]
  158. Poeker SA, Geirnaert A, Berchtold L, Greppi A, Krych L et al. Understanding the prebiotic potential of different dietary fibers using an in vitro continuous adult fermentation model (PolyFermS). Sci Rep 2018; 8:4318 [View Article] [PubMed]
    [Google Scholar]
  159. Xu Y, Wang Y, Li H, Dai Y, Chen D et al. Altered fecal microbiota composition in older adults with frailty. Front Cell Infect Microbiol 2021; 11:744 [View Article]
    [Google Scholar]
  160. Reichardt N, Duncan SH, Young P, Belenguer A, McWilliam Leitch C et al. Phylogenetic distribution of three pathways for propionate production within the human gut microbiota. ISME J 2014; 8:1323–1335 [View Article] [PubMed]
    [Google Scholar]
  161. Chiappori F, Cupaioli FA, Consiglio A, Di Nanni N, Mosca E et al. Analysis of faecal microbiota and small ncRNAs in autism: detection of miRNAs and piRNAs with possible implications in host–gut microbiota cross-talk. Nutrients 2022; 14:1340 [View Article]
    [Google Scholar]
  162. Heinken A, Khan MT, Paglia G, Rodionov DA, Harmsen HJM et al. Functional metabolic map of Faecalibacterium prausnitzii, a beneficial human gut microbe. J Bacteriol 2014; 196:3289–3302 [View Article]
    [Google Scholar]
  163. Spychala MS, Venna VR, Jandzinski M, Doran SJ, Durgan DJ et al. Age-related changes in the gut microbiota influence systemic inflammation and stroke outcome. Ann Neurol 2018; 84:23–36 [View Article] [PubMed]
    [Google Scholar]
  164. Louis P, Flint HJ. Formation of propionate and butyrate by the human colonic microbiota. Environ Microbiol 2017; 19:29–41 [View Article] [PubMed]
    [Google Scholar]
  165. Chen H-M, Chung Y-CE, Chen H-C, Liu Y-W, Chen I-M et al. Exploration of the relationship between gut microbiota and fecal microRNAs in patients with major depressive disorder. Sci Rep 2022; 12:20977 [View Article] [PubMed]
    [Google Scholar]
  166. Saraswati S, Sitaraman R. Aging and the human gut microbiota-from correlation to causality. Front Microbiol 2014; 5:764 [View Article] [PubMed]
    [Google Scholar]
  167. La-Ongkham O, Nakphaichit M, Nakayama J, Keawsompong S, Nitisinprasert S et al. Age-related changes in the gut microbiota and the core gut microbiome of healthy thai humans. 3 Biotech 2020; 10:1–14
    [Google Scholar]
  168. Cui Y, Zhang L, Wang X, Yi Y, Shan Y. Roles of intestinal Parabacteroides in human health and diseases. FEMS Microbiol Lett 2022; 369:fnac072 [View Article]
    [Google Scholar]
  169. Meng C, Feng S, Hao Z, Dong C, Liu H. Changes in gut microbiota composition with age and correlations with gut inflammation in rats. PLoS One 2022; 17:e0265430 [View Article] [PubMed]
    [Google Scholar]
  170. Kato K, Odamaki T, Mitsuyama E, Sugahara H, Xiao J-Z et al. Age-related changes in the composition of gut Bifidobacterium species. Curr Microbiol 2017; 74:987–995 [View Article] [PubMed]
    [Google Scholar]
  171. Rivière A, Selak M, Lantin D, Leroy F, De Vuyst L. Bifidobacteria and butyrate-producing colon bacteria: importance and strategies for their stimulation in the human gut. Front Microbiol 2016; 7:979 [View Article] [PubMed]
    [Google Scholar]
  172. Devika NT, Raman K. Deciphering the metabolic capabilities of Bifidobacteria using genome-scale metabolic models. Sci Rep 2019; 9:18222 [View Article] [PubMed]
    [Google Scholar]
  173. Parada Venegas D, De la Fuente MK, Landskron G, González MJ, Quera R et al. Short Chain Fatty Acids (SCFAs)-mediated gut epithelial and immune regulation and its relevance for inflammatory bowel diseases. Front Immunol 2019; 10:277 [View Article]
    [Google Scholar]
  174. Duranti S, Ruiz L, Lugli GA, Tames H, Milani C et al. Bifidobacterium adolescentis as a key member of the human gut microbiota in the production of GABA. Sci Rep 2020; 10:14112 [View Article] [PubMed]
    [Google Scholar]
  175. Chen S, Chen L, Qi Y, Xu J, Ge Q et al. Bifidobacterium adolescentis regulates catalase activity and host metabolism and improves healthspan and lifespan in multiple species. Nat Aging 2021; 1:991–1001 [View Article]
    [Google Scholar]
  176. Arboleya S, Watkins C, Stanton C, Ross RP. Gut Bifidobacteria populations in human health and aging. Front Microbiol 2016; 7:1204 [View Article]
    [Google Scholar]
  177. Faghfoori Z, Faghfoori MH, Saber A, Izadi A, Yari Khosroushahi A. Anticancer effects of Bifidobacteria on colon cancer cell lines. Cancer Cell Int 2021; 21:258 [View Article] [PubMed]
    [Google Scholar]
  178. Wu C-S, Muthyala SDV, Klemashevich C, Ufondu AU, Menon R et al. Age-dependent remodeling of gut microbiome and host serum metabolome in mice. Aging 2021; 13:6330–6345 [View Article] [PubMed]
    [Google Scholar]
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