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Manuscript ID : SJOAPB-2210-1396 (R1) Visit : 204 Page: 59 - 86

Article Type: Original Research

The importance of short chain fatty acids synthesized by intestinal microorganisms, as an epigenetic factor, in reducing the incidence of colon cancer

Subject Areas : genetic

Shiva  Darabi 1 (Ph.D. Student, Department of Biology, Sanandaj Branch, Islamic Azad University, Sanandaj, Iran)
Fatemeh  Keshavarzi 2 (Associate Professor, Department of Biology, Sanandaj Branch, Islamic Azad University, Sanandaj, Iran)
parviz  Ahtari 3 (Associate Professor, Radiation Application Research School, Nuclear Science and Technology Research Institute (NSTRI), Karaj, Iran)
Farahnaz  Motamedi Sedeh 4 (Associate Professor, Department of Veterinary and Animal Science, Nuclear Agriculture Research School, Nuclear Science and Technology Research Institute, Karaj, Iran)
Behrouz  Alirezapour 5 (Associate Professor, Radiation Applications Research School, Nuclear Science and Technology Research Institute, Tehran, Iran)

Received: 2022-04-10 Accepted : 2022-06-06 Published : 2022-06-22

Keywords: short chain fatty acids (SCFAs), Diet, Epigenetic factors,  Gut microbiota, Colon cancer,

Abstract :

Objective: The mechanisms involved in the pathogenesis of colorectal cancer are still not well understood, but diet is the main factor that has multifaceted effects, including changes in the host's metabolome and transcriptome. Metabolites obtained from diet can directly affect the metabolism of the whole body. The purpose ofthis study is to review the effect of intestinal microbiota through the synthesis ofshort chain fatty acids (acetate, butyrate and propionate), and as a result, the induction of cytochrome P4501A1 gene expression in the prevention and treatment of colon cancer.Materials and methods: Using keywords, searching and collecting articles from PubMed and citation databases, I.S. I. (ISI web of Knowledge), SCOPUS, Google Scholar, ProQuest, Oxford and Ovid, as well as the most famous internal databases including the Academic Jihad Database (SID), Iranmedex, Magiran, Irandoc and MedLib were performed.Findings: Undigested food ingredients that enter the large intestine are fermented by intestinal microbiota and fermentative metabolites are produced that perform a wide range of effective functions. Some of these metabolites interact with the intestinal immune system, including short-chain fatty acids, aryl hydrocarbon receptor ligands, and bile acid metabolites that play a role in inducing intestinal immune homeostasis.It seems that the protective effects of short chain fatty acids synthesized by microorganisms, in colon cancer by inhibiting the activity of histone deacetylase and strengthening the aryl hydrocarbon receptor and thus protecting DNA against damage caused by carcinogens, by activating xenobiotic metabolizing enzymes, such as Cytochrome P4501A1, apply.Conclusion: The present study presented a new perspective regarding the importance of intestinal microbiota through the production of short chain fatty acids, especially acetate, butyrate and propionate, as medicinal targets for the prevention and even treatment of colorectal cancer.

References:


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_||_

  1. Zheng P, Li Zh & Zhou Zh. Gut microbiome in type 1 diabetes: A comprehensive review. Diabetes Metab Res Rev. 2018; 34: e3043. DOI:org/10.1002/dmrr.3043
    2.
  2. Poppe J, Baarle L, Matteoli G & Verbeke K. How microbial food fermentation supports a tolerant gut. Molecular Nutrition & Food Research. 2020. DOI: 1002/mnfr.202000036
    3.
  3. Mayer EA, Savidge T & Shulman RJ. Brain-gut microbiome interactions and functional bowel disorders. Gastroenterology. 2014; 146:1500-12.
    DOI: 1053/j.gastro.2014.02.037
    4.
  4. Macfarlane, GT & Macfarlane, S. Bacteria,colonic fermentation and gastro intestinal health. AOAC Int. 2012; 95: 50-60.
    5.
  5. Xu W, Zhou Y & Hang X, Shen D. Current evidence on the relationship between CYP1B1 polymorphisms and lung cancer risk: a metaanalysis. Mol Biol Rep. 2012; 39(3): 2821-9.
    6.
  6. Beyerle J, Frei E, Stiborov M, Habermann N & Ulrich CM. Biotransformation of xenobiotics in the human colon and rectum and its association with colorectal cancer. Drug Metab Rev; 2015; 47: 199-221.
    7.
  7. Gutierrez-Vazquez C & Quintana FJ. Regulation of the immune response by the aryl hydrocarbon receptor. Immunity. 2018; 48(1): 19-33.
    8.
  8. Donaldson GP, Lee SM & Mazmanian SK. Gut biogeography of the bacterial microbiota. Nature reviews. Microbiology. 2016; 14(1): 20-32.
    9.
  9. Li H & et al. The outer mucus layer hosts a distinct intestinal microbial niche. Nature Communications. 2015; 6(1): 8292.
    10.
  10. Franzosa EA & et al. Identifying personal microbiomes using metagenomic codes. Proceedings of the National Academy of Sciences of the United States of America. 2015; 112(22): 2930-8.
    11.
  11. Costea PI & et al. Enterotypes in the landscape of gut microbial community composition. Nature Microbiology. 2017; 3(1): 8-16.
    12.
  12. Ha CW, Lam YY & Holmes AJ. Mechanistic links between gut microbial community dynamics, microbial functions and metabolic health. World Journal of Gastroenterology. 2014; 20(44): 16498-16517.
    13.
  13. Marinelli L, Martin-Gallausiaux C, Bourhis J-M, B_eguet-Crespel F, Blotti_ere HM & Lapaque N. Identification of the novel role of butyrate as Ahr ligand in human intestinal epithelial cells. Sci Rep. 2019; 9(1): 643.
    14.
  14. Van der Beek CM & et al. Distal, not proximal, colonic acetate infusions promote fat oxidation and improve metabolic markers in overweight/obese men. Clin Sci (Lond). 2016; 130(22): 2073-2082. DOI:1042/CS20160263
    15.
  15. Louis P, Hold G & Flint HJ.The gut microbiota, bacterial metabolites and colorectal cancer. Rev.Microbiol. 2014; 12: 661-672. DOI: 10.1038/nrmicro3344
    16.
  16. Reichardt N & et al. Phylogenetic distribution of three pathways forpropionate production within the human gut microbiota. ISMEJ. 2014; 8: 1323-1335.
    DOI:1038/ismej.2014.14
    17.
  17. Flint HJ, Duncan SH, Scott KP, & Louis P. Links between diet, gut microbiota composition and gut Proc.Nutr.Soc. 2015; 74:13-22.
    DOI: 10.1017/s0029665114001463
    18.
  18. Machiels K, & et al. Adecrease of the butyrate-producing species Roseburiahominis and Faecali bacterium prausnitzii defines dysbiosis in patients with Gut. 2014; 63:1275-1283. DOI: 10.1136/gutjnl-2013-304833.
    19.
  19. Nedjadi T, Moran, AW, Al-Rammahi MA & Shirazi-Beechey SP. Characterization of butyrate transport across the luminal membranes of equine large intestine. Exp Physiol. 2014; 99(10): 1335-1347.
    20.
  20. Boets E, Deroover L, Houben E, Vermeulen K, Gomand SV, Delcour JA & Verbeke K. Quantification of in vivo colonic short chain fatty acid production from inulin. Nutrients. 2015; 7(11): 8916-8929.
    21.
  21. Macfarlane GT & Macfarlane S. Bacteria,colonic fermentation and gastro intestinal health. AOACInt. 2012; 95: 50-60.
    22.
  22. Jung TH, Park JH, Jeon WM & Han KS. Butyrate modulates bacterial adherence on LS174T human colorectal cells by stimulating mucin secretionand MAPK signaling pathway. Res.Pract. 2015; 9: 343-349. DOI: 10.4162/nrp.2015.9.4.343
    23.
  23. Den Besten G & et al. Short-chain fatty acids protect against high-fatdiet-induced obesity via a PPAR gamma-Dependent Switch from lipogenesist of at oxidation. 2015; 64: 2398-2408. DOI: 10.2337/db14-1213
    24.
  24. Canfora EE., Jocken JW. & Blaak EE. Short-chain fatty acids in control of body weight and insulin sensitivity. Rev.Endocrinol. 2015, 11: 577-591.     
    DOI: 10.1038/nrendo.2015.128.
    25.
  25. Keku TO, Dulal S, Deveaux A, Jovov, B & Han X. The gastro intestinal microbiota and colorectal cancer. J. Physiol. Gastrointest. LiverPhysiol. 2015, 308: G351-G363.
    DOI: 10.1152/ajpgi.00360.2012
    26.
  26. Simon GM, Cheng J & Gordon JI. Quantitative assessment of the impact of the gut microbiota on lysine -acetylation of host proteins using gnotobiotic mice. Proceedings of the National Academy of Sciences. 2012; 109(28): 11133-11138.
    27.
  27. Xie Z & et al. Metabolic Regulation of Gene Expression by Histone Lysine β-Hydroxybutyrylation. Molecular Cell. 2016; 62(2): 194-206.
    28.
  28. Fellows R & et al. Microbiota derived short chain fatty acids promote histone crotonylation in the colon through histone deacetylases. Nature Communications. 2018; 9(1): 105.
    29.
  29. Wang G & et al. Role of SCFAs in gut microbiome and glycolysis for colorectal cancer therapy. Journal of cellular physiology. 2019. DOI:1002/jcp.28436.
    30.
  30. Han A, Bennett N, Macdonald A, Johnstone M, Whelan J & Donohoe DR. Cellular metabolism and dose reveal carnitine‐dependent and ‐independent mechanisms of butyrate oxidation in colorectal cancer cells. Journal of Cellular Physiology. 2016; 231: 1804-1813.
    31.
  31. Koh A, De VF, Kovatcheva‐Datchary P & Bckhed F. From dietary fiber to host physiology: Short‐chain fatty acids as key bacterial metabolites. Cell. 2016; 165:
    1332-1345.
    32.
  32. Zheng L & et al. Microbial-Derived Butyrate Promotes Epithelial Barrier Function through IL-10 Receptor–Dependent Repression of Claudin-2. The Journal of Immunology. 2017; 199(8): 2976-2984. DOI:4049/jimmunol.1700105
    33.
  33. Binoy Shivanna, Ch Ch & Bhagavatula M. The Aryl Hydrocarbon Receptor (AHR): A Novel Therapeutic Target for Pulmonary Diseases? J. Mol. Sci. 2022; 23: 1516.
    DOI: https://doi.org/1 0.3390/ijms23031516
    34.
  34. Agus A, Planchais J & Sokol H. Gut Microbiota Regulation of Tryptophan Metabolism in Health and Disease. Cell Host Microbe. 2018; 23: 716-724.
    35.
  35. Gutierrez-Vazquez C & Quintana FJ. Regulation of the immune response by the aryl hydrocarbon receptor. Immunity. 2018; 48(1): 19-33.
    36.
  36. Roager HM & Licht TR. Microbial tryptophan catabolites in health and disease. Commun. 2018; 9: 3294.
    37.
  37. Korecka A & et al. Bidirectional communication between the Aryl hydrocarbon Receptor (AhR) and the microbiome tunes host metabolism. NPJ Biofilms Microbiomes. 2016; 2: 16014.
    38.
  38. Cibrian D & et al. CD69 controls the uptake of L-tryptophan through LAT1-CD98 and AhR-dependent secretion of IL-22 in psoriasis. Immunol. 2016; 17: 985-996.
    39.
  39. Vyhlídalová B & et al. Gut Microbial Catabolites of Tryptophan Are Ligands and Agonists of the Aryl Hydrocarbon Receptor: A Detailed Characterization. J. Mol. Sci. 2020; 21: 2614.
    40.
  40. Zhang M & et al. The Chinese medicinal herb decoction QRZSLXF enhances anti-inflammatory e_ect in TNBS-induced colitis via balancing Th17/Tregs J. Ethnopharmacol. 2020; 251: 112549.
    41.
  41. Jin UH & et al. Short Chain Fatty Acids Enhance Aryl Hydrocarbon (Ah) Responsiveness in Mouse Colonocytes and Caco-2 Human Colon Cancer Cells. Rep. 2017; 7: 10163.
    42.
  42. Piper CJM & et al. Aryl Hydrocarbon Receptor Contributes to the Transcriptional Program of IL-10 Producing Regulatory B Cells. Cell Rep. 2019; 29: 1878-1892.e7.
    43.
  43. Manzella CR & et al. Serotonin Modulates AhR Activation by Interfering with CYP1A1-Mediated Clearance of AhR Ligands. Cell Physiol. Biochem. 2020; 54: 126-141.
    44.
  44. Obata Y & et al. Neuronal programming by microbiota regulates intestinal physiology. Nature, 2020; 578: 284-289.
    45.
  45. Zapletal O & et al. Butyrate alters expression of cytochrome P450 1A1 and metabolism of benzoapyrene via its histone deacetylase activity in colon epithelial cell models. Toxicol. 2017; 91: 2135-2150.
    46.
  46. Rosser EC & et al. Microbiota-DerivedMetabolites SuppressArthritis byAmplifyingAryl-Hydrocarbon Receptor Activation in Regulatory B Cells. CellMetab. 2020; 31:
    837-851.e10.
    47.
  47. Wang J & et al. Aryl hydrocarbon receptor/IL-22/Stat3 signaling pathway is involved in the modulation of intestinal mucosa antimicrobial molecules by commensal microbiota in mice. Innate Immun. 2018; 24: 297-306.
    48.
  48. Collins SL & Patterson AD. The gut microbiome: an orchestrator of xenobiotic metabolism. Acta Pharmaceutica Sinica B. 2020; 10(1): 19e32.
    49.
  49. Un-Ho Jin & et al. Short Chain Fatty Acids Enhance Aryl Hydrocarbon (Ah) Responsiveness in Mouse Colonocytes and Caco-2 Human Colon Cancer Cells. ScienTiFic REPortS. 2017; 7: 10163. DOI: 1038/s41598-017-10824-x
    50.
  50. Jin UH & et al. Microbiome-derived tryptophan metabolites and their aryl hydrocarbon receptor-dependent agonist and antagonist activities. Pharmacol. 2014; 85: 777-788.
    51.
  51. Cheng Y & et al. Editor’s Highlight: Microbial-Derived 1,4-Dihydroxy-2-naphthoic Acid and Related Compounds as Aryl Hydrocarbon Receptor Agonists/Antagonists: Structure-Activity Relationships and Receptor Modeling. Sci. 2017; 155: 458-473.
    52.
  52. Metidji A & et al. The environmental sensor Ahr protects from inflammatory damage by maintaining intestinal stem cell homeostasis and barrier integrity. Immunity. 2018; 49(2): 353-362 e355.
    53.

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