DOI QR코드

DOI QR Code

The interaction between gut microbiome and nutrients on development of human disease through epigenetic mechanisms

  • Lee, Ho-Sun (Forensic Toxicology Division, Daegu Institute, National Forensic Service)
  • 투고 : 2019.09.04
  • 심사 : 2019.09.22
  • 발행 : 2019.09.30

초록

Early environmental exposure is recognized as a key factor for long-term health based on the Developmental Origins of Health and Disease hypothesis. It considers that early-life nutrition is now being recognized as a major contributor that may permanently program change of organ structure and function toward the development of diseases, in which epigenetic mechanisms are involved. Recent researches indicate early-life environmental factors modulate the microbiome development and the microbiome might be mediate diet-epigenetic interaction. This review aims to define which nutrients involve microbiome development during the critical window of susceptibility to disease, and how microbiome modulation regulates epigenetic changes and influences human health and future prevention strategies.

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참고문헌

  1. Barker DJ, Osmond C. Infant mortality, childhood nutrition, and ischaemic heart disease in England and Wales. Lancet 1986;1:1077-1081. https://doi.org/10.1016/S0140-6736(86)91340-1
  2. Lee HS. Impact of maternal diet on the epigenome during In utero life and the developmental programming of diseases in childhood and adulthood. Nutrients 2015;7:9492-9507. https://doi.org/10.3390/nu7115467
  3. Stiemsma LT, Michels KB. The role of the microbiome in the developmental origins of health and disease. Pediatrics 2018;141:e20172437. https://doi.org/10.1542/peds.2017-2437
  4. Vineis P, Chatziioannou A, Cunliffe VT, Flanagan JM, Hanson M, Kirsch-Volders M, et al. Epigenetic memory in response to environmental stressors. FASEB J 2017;31:2241-2251. https://doi.org/10.1096/fj.201601059RR
  5. Reid MA, Dai Z, Locasale JW. The impact of cellular metabolism on chromatin dynamics and epigenetics. Nat Cell Biol 2017;19:1298-1306. https://doi.org/10.1038/ncb3629
  6. Bannister AJ, Kouzarides T. Regulation of chromatin by histone modifications. Cell Res 2011;21:381-395. https://doi.org/10.1038/cr.2011.22
  7. Ho NT, Li F, Lee-Sarwar KA, Tun HM, Brown BP, Pannaraj PS, et al. Meta-analysis of effects of exclusive breastfeeding on infant gut microbiota across populations. Nat Commun 2018;9:4169. https://doi.org/10.1038/s41467-018-06473-x
  8. Korpela K, Blakstad EW, Moltu SJ, Strommen K, Nakstad B, Ronnestad AE, et al. Intestinal microbiota development and gestational age in preterm neonates. Sci Rep 2018;8:2453. https://doi.org/10.1038/s41598-018-20827-x
  9. Blanc RS, Richard S. Arginine methylation: the coming of age. Mol Cell 2017;65:8-24. https://doi.org/10.1016/j.molcel.2016.11.003
  10. Qin Y, Roberts JD, Grimm SA, Lih FB, Deterding LJ, Li R, et al. An obesity-associated gut microbiome reprograms the intestinal epigenome and leads to altered colonic gene expression. Genome Biol 2018;19:7. https://doi.org/10.1186/s13059-018-1389-1
  11. Costantini L, Molinari R, Farinon B, Merendino N. Impact of omega-3 fatty acids on the gut microbiota. Int J Mol Sci 2017;18:E2645.
  12. van Dijk SJ, Zhou J, Peters TJ, Buckley M, Sutcliffe B, Oytam Y, et al. Effect of prenatal DHA supplementation on the infant epigenome: results from a randomized controlled trial. Clin Epigenetics 2016;8:114. https://doi.org/10.1186/s13148-016-0281-7
  13. Ma J, Prince AL, Bader D, Hu M, Ganu R, Baquero K, et al. High-fat maternal diet during pregnancy persistently alters the offspring microbiome in a primate model. Nat Commun 2014;5:3889. https://doi.org/10.1038/ncomms4889
  14. Kang I, Kim Y, Tomas-Barberan FA, Espin JC, Chung S. Urolithin A, C, and D, but not iso-urolithin A and urolithin B, attenuate triglyceride accumulation in human cultures of adipocytes and hepatocytes. Mol Nutr Food Res 2016;60:1129-1138. https://doi.org/10.1002/mnfr.201500796
  15. Kang I, Buckner T, Shay NF, Gu L, Chung S. Improvements in metabolic health with consumption of ellagic acid and subsequent conversion into urolithins: evidence and mechanisms. Adv Nutr 2016;7:961-972. https://doi.org/10.3945/an.116.012575
  16. Zhang Z, Chen Y, Xiang L, Wang Z, Xiao GG, Hu J. Effect of curcumin on the diversity of gut microbiota in ovariectomized rats. Nutrients 2017;9:E1146.
  17. Stiemsma LT, Turvey SE. Asthma and the microbiome: defining the critical window in early life. Allergy Asthma Clin Immunol 2017;13:3. https://doi.org/10.1186/s13223-016-0173-6
  18. Salminen A, Kauppinen A, Hiltunen M, Kaarniranta K. Krebs cycle intermediates regulate DNA and histone methylation: epigenetic impact on the aging process. Ageing Res Rev 2014;16:45-65. https://doi.org/10.1016/j.arr.2014.05.004
  19. Cardaci S, Ciriolo MR. TCA cycle defects and cancer: when metabolism tunes redox state. Int J Cell Biol 2012;2012:161837. https://doi.org/10.1155/2012/161837
  20. Mentch SJ, Mehrmohamadi M, Huang L, Liu X, Gupta D, Mattocks D, et al. Histone methylation dynamics and gene regulation occur through the sensing of one-carbon metabolism. Cell Metab 2015;22:861-873. https://doi.org/10.1016/j.cmet.2015.08.024
  21. Inagaki T, Tachibana M, Magoori K, Kudo H, Tanaka T, Okamura M, et al. Obesity and metabolic syndrome in histone demethylase JHDM2a-deficient mice. Genes Cells 2009;14:991-1001. https://doi.org/10.1111/j.1365-2443.2009.01326.x
  22. Tateishi K, Okada Y, Kallin EM, Zhang Y. Role of Jhdm2a in regulating metabolic gene expression and obesity resistance. Nature 2009;458:757-761. https://doi.org/10.1038/nature07777
  23. Hino S, Nagaoka K, Nakao M. Metabolism-epigenome crosstalk in physiology and diseases. J Hum Genet 2013;58:410-415. https://doi.org/10.1038/jhg.2013.57
  24. Janssen JJ, Grefte S, Keijer J, de Boer VC. Mito-nuclear communication by mitochondrial metabolites and its regulation by B-vitamins. Front Physiol 2019;10:78. https://doi.org/10.3389/fphys.2019.00078
  25. Tzika E, Dreker T, Imhof A. Epigenetics and metabolism in health and disease. Front Genet 2018;9:361. https://doi.org/10.3389/fgene.2018.00361
  26. Xu W, Li Y, Liu C, Zhao S. Protein lysine acetylation guards metabolic homeostasis to fight against cancer. Oncogene 2014;33:2279-2285. https://doi.org/10.1038/onc.2013.163
  27. Liang F, Kume S, Koya D. SIRT1 and insulin resistance. Nat Rev Endocrinol 2009;5:367-373. https://doi.org/10.1038/nrendo.2009.101
  28. Eckel-Mahan KL, Patel VR, de Mateo S, Orozco-Solis R, Ceglia NJ, Sahar S, et al. Reprogramming of the circadian clock by nutritional challenge. Cell 2013;155:1464-1478. https://doi.org/10.1016/j.cell.2013.11.034
  29. Aguilar-Arnal L, Sassone-Corsi P. Chromatin landscape and circadian dynamics: Spatial and temporal organization of clock transcription. Proc Natl Acad Sci U S A 2015;112:6863-6870. https://doi.org/10.1073/pnas.1411264111
  30. Navarro E, Funtikova AN, Fito M, Schroder H. Prenatal nutrition and the risk of adult obesity: long-term effects of nutrition on epigenetic mechanisms regulating gene expression. J Nutr Biochem 2017;39:1-14. https://doi.org/10.1016/j.jnutbio.2016.03.012
  31. Terasaka T, Otsuka F, Tsukamoto N, Nakamura E, Inagaki K, Toma K, et al. Mutual interaction of kisspeptin, estrogen and bone morphogenetic protein-4 activity in GnRH regulation by GT1-7 cells. Mol Cell Endocrinol 2013;381:8-15. https://doi.org/10.1016/j.mce.2013.07.009
  32. Hardiville S, Hart GW. Nutrient regulation of gene expression by O-GlcNAcylation of chromatin. Curr Opin Chem Biol 2016;33:88-94. https://doi.org/10.1016/j.cbpa.2016.06.005
  33. Olivier-Van Stichelen S, Wang P, Comly M, Love DC, Hanover JA. Nutrient-driven O-linked N-acetylglucosamine (O-GlcNAc) cycling impacts neurodevelopmental timing and metabolism. J Biol Chem 2017;292:6076-6085. https://doi.org/10.1074/jbc.M116.774042
  34. Li MD, Vera NB, Yang Y, Zhang B, Ni W, Ziso-Qejvanaj E, et al. Adipocyte OGT governs diet-induced hyperphagia and obesity. Nat Commun 2018;9:5103. https://doi.org/10.1038/s41467-018-07461-x
  35. Qin J, Li Y, Cai Z, Li S, Zhu J, Zhang F, et al. A metagenome-wide association study of gut microbiota in type 2 diabetes. Nature 2012;490:55-60. https://doi.org/10.1038/nature11450
  36. Perry RJ, Peng L, Barry NA, Cline GW, Zhang D, Cardone RL, et al. Acetate mediates a microbiome-brain-beta-cell axis to promote metabolic syndrome. Nature 2016;534:213-217. https://doi.org/10.1038/nature18309
  37. Turnbaugh PJ, Ley RE, Mahowald MA, Magrini V, Mardis ER, Gordon JI. An obesity-associated gut microbiome with increased capacity for energy harvest. Nature 2006;444:1027-1031. https://doi.org/10.1038/nature05414
  38. Tanca A, Abbondio M, Palomba A, Fraumene C, Manghina V, Cucca F, et al. Potential and active functions in the gut microbiota of a healthy human cohort. Microbiome 2017;5:79. https://doi.org/10.1186/s40168-017-0293-3
  39. DiGiulio DB, Romero R, Amogan HP, Kusanovic JP, Bik EM, Gotsch F, et al. Microbial prevalence, diversity and abundance in amniotic fluid during preterm labor: a molecular and culture-based investigation. PLoS One 2008;3:e3056 https://doi.org/10.1371/journal.pone.0003056
  40. Perez-Munoz ME, Arrieta MC, Ramer-Tait AE, Walter J. A critical assessment of the “sterile womb” and “in utero colonization” hypotheses: implications for research on the pioneer infant microbiome. Microbiome 2017;5:48. https://doi.org/10.1186/s40168-017-0268-4
  41. Milani C, Duranti S, Bottacini F, Casey E, Turroni F, Mahony J, et al. The first microbial colonizers of the human gut: composition, activities, and health implications of the infant gut microbiota. Microbiol Mol Biol Rev 2017;81:e00036-17.
  42. Kristensen K, Henriksen L. Cesarean section and disease associated with immune function. J Allergy Clin Immunol 2016;137:587-590. https://doi.org/10.1016/j.jaci.2015.07.040
  43. Huh SY, Rifas-Shiman SL, Zera CA, Edwards JW, Oken E, Weiss ST, et al. Delivery by caesarean section and risk of obesity in preschool age children: a prospective cohort study. Arch Dis Child 2012;97:610-616. https://doi.org/10.1136/archdischild-2011-301141
  44. Schlinzig T, Johansson S, Gunnar A, Ekstrom TJ, Norman M. Epigenetic modulation at birth - altered DNA-methylation in white blood cells after Caesarean section. Acta Paediatr 2009;98:1096-1099. https://doi.org/10.1111/j.1651-2227.2009.01371.x
  45. Almgren M, Schlinzig T, Gomez-Cabrero D, Gunnar A, Sundin M, Johansson S, et al. Cesarean delivery and hematopoietic stem cell epigenetics in the newborn infant: implications for future health? Am J Obstet Gynecol 2014;211:502.
  46. Arboleya S, Binetti A, Salazar N, Fernandez N, Solis G, Hernandez-Barranco A, et al. Establishment and development of intestinal microbiota in preterm neonates. FEMS Microbiol Ecol 2012;79:763-772. https://doi.org/10.1111/j.1574-6941.2011.01261.x
  47. Rossi M, Amaretti A, Raimondi S. Folate production by probiotic bacteria. Nutrients 2011;3:118-134. https://doi.org/10.3390/nu3010118
  48. Tamburini S, Shen N, Wu HC, Clemente JC. The microbiome in early life: implications for health outcomes. Nat Med 2016;22:713-722. https://doi.org/10.1038/nm.4142
  49. Hullar MA, Fu BC. Diet, the gut microbiome, and epigenetics. Cancer J 2014;20:170-175. https://doi.org/10.1097/PPO.0000000000000053
  50. Gerhauser C. Impact of dietary gut microbial metabolites on the epigenome. Philos Trans R Soc Lond B Biol Sci 2018;373:20170359. https://doi.org/10.1098/rstb.2017.0359
  51. Krautkramer KA, Dhillon RS, Denu JM, Carey HV. Metabolic programming of the epigenome: host and gut microbial metabolite interactions with host chromatin. Transl Res 2017;189:30-50. https://doi.org/10.1016/j.trsl.2017.08.005
  52. Yoshii K, Hosomi K, Sawane K, Kunisawa J. Metabolism of dietary and microbial vitamin B family in the regulation of host immunity. Front Nutr 2019;6:48. https://doi.org/10.3389/fnut.2019.00048
  53. Dalile B, Van Oudenhove L, Vervliet B, Verbeke K. The role of short-chain fatty acids in microbiota-gut-brain communication. Nat Rev Gastroenterol Hepatol 2019;16:461-478. https://doi.org/10.1038/s41575-019-0157-3
  54. Thorburn AN, McKenzie CI, Shen S, Stanley D, Macia L, Mason LJ, et al. Evidence that asthma is a developmental origin disease influenced by maternal diet and bacterial metabolites. Nat Commun 2015;6:7320. https://doi.org/10.1038/ncomms8320
  55. Shimazu T, Hirschey MD, Newman J, He W, Shirakawa K, Le Moan N, et al. Suppression of oxidative stress by beta-hydroxybutyrate, an endogenous histone deacetylase inhibitor. Science 2013;339:211-214. https://doi.org/10.1126/science.1227166
  56. Luu M, Pautz S, Kohl V, Singh R, Romero R, Lucas S, et al. The short-chain fatty acid pentanoate suppresses autoimmunity by modulating the metabolic-epigenetic crosstalk in lymphocytes. Nat Commun 2019;10:760. https://doi.org/10.1038/s41467-019-08711-2
  57. Vazquez-Gomez M, Garcia-Contreras C, Torres-Rovira L, Pesantez JL, Gonzalez-Anover P, Gomez-Fidalgo E, et al. Polyphenols and IUGR pregnancies: maternal hydroxytyrosol supplementation improves prenatal and early-postnatal growth and metabolism of the offspring. PLoS One 2017;12:e0177593. https://doi.org/10.1371/journal.pone.0177593
  58. Wu S, Tian L. Diverse phytochemicals and bioactivities in the ancient fruit and modern functional food pomegranate (Punica granatum). Molecules 2017;22:E1606.
  59. Tomas-Barberan FA, Selma MV, Espin JC. Interactions of gut microbiota with dietary polyphenols and consequences to human health. Curr Opin Clin Nutr Metab Care 2016;19:471-476. https://doi.org/10.1097/MCO.0000000000000314
  60. Selma MV, Beltran D, Luna MC, Romo-Vaquero M, Garcia-Villalba R, Mira A, et al. Isolation of human intestinal bacteria capable of producing the bioactive metabolite isourolithin A from ellagic acid. Front Microbiol 2017;8:1521. https://doi.org/10.3389/fmicb.2017.01521
  61. Thakur VS, Gupta K, Gupta S. Green tea polyphenols increase p53 transcriptional activity and acetylation by suppressing class I histone deacetylases. Int J Oncol 2012;41:353-361.
  62. Lee HS, Barraza-Villarreal A, Hernandez-Vargas H, Sly PD, Biessy C, Ramakrishnan U, et al. Modulation of DNA methylation states and infant immune system by dietary supplementation with omega-3 PUFA during pregnancy in an intervention study. Am J Clin Nutr 2013;98:480-487. https://doi.org/10.3945/ajcn.112.052241
  63. Robertson RC, Kaliannan K, Strain CR, Ross RP, Stanton C, Kang JX. Maternal omega-3 fatty acids regulate offspring obesity through persistent modulation of gut microbiota. Microbiome 2018;6:95. https://doi.org/10.1186/s40168-018-0476-6
  64. Whitt J, Woo V, Lee P, Moncivaiz J, Haberman Y, Denson L, et al. Disruption of epithelial HDAC3 in intestine prevents diet-induced obesity in mice. Gastroenterology 2018;155:501-513. https://doi.org/10.1053/j.gastro.2018.04.017
  65. Hsu CN, Hou CY, Lee CT, Chan JY, Tain YL. The interplay between maternal and post-weaning high-fat diet and gut microbiota in the developmental programming of hypertension. Nutrients 2019;11:E1982.
  66. Parlee SD, MacDougald OA. Maternal nutrition and risk of obesity in offspring: the Trojan horse of developmental plasticity. Biochim Biophys Acta 2014;1842:495-506. https://doi.org/10.1016/j.bbadis.2013.07.007
  67. Turnbaugh PJ, Hamady M, Yatsunenko T, Cantarel BL, Duncan A, Ley RE, et al. A core gut microbiome in obese and lean twins. Nature 2009;457:480-484. https://doi.org/10.1038/nature07540
  68. Connor KL, Chehoud C, Altrichter A, Chan L, DeSantis TZ, Lye SJ. Maternal metabolic, immune, and microbial systems in late pregnancy vary with malnutrition in mice. Biol Reprod 2018;98:579-592.
  69. Stanislawski MA, Dabelea D, Wagner BD, Sontag MK, Lozupone CA, Eggesbo M. Pre-pregnancy weight, gestational weight gain, and the gut microbiota of mothers and their infants. Microbiome 2017;5:113. https://doi.org/10.1186/s40168-017-0332-0
  70. Vatanen T, Kostic AD, d'Hennezel E, Siljander H, Franzosa EA, Yassour M, et al. Variation in microbiome LPS immunogenicity contributes to autoimmunity in humans. Cell 2016;165:1551. https://doi.org/10.1016/j.cell.2016.05.056
  71. Wankhade UD, Zhong Y, Kang P, Alfaro M, Chintapalli SV, Thakali KM, et al. Enhanced offspring predisposition to steatohepatitis with maternal high-fat diet is associated with epigenetic and microbiome alterations. PLoS One 2017;12:e0175675. https://doi.org/10.1371/journal.pone.0175675
  72. Soderborg TK, Clark SE, Mulligan CE, Janssen RC, Babcock L, Ir D, et al. The gut microbiota in infants of obese mothers increases inflammation and susceptibility to NAFLD. Nat Commun 2018;9:4462. https://doi.org/10.1038/s41467-018-06929-0
  73. Chu DM, Antony KM, Ma J, Prince AL, Showalter L, Moller M, et al. The early infant gut microbiome varies in association with a maternal high-fat diet. Genome Med 2016;8:77. https://doi.org/10.1186/s13073-016-0330-z
  74. Aagaard-Tillery KM, Grove K, Bishop J, Ke X, Fu Q, McKnight R, et al. Developmental origins of disease and determinants of chromatin structure: maternal diet modifies the primate fetal epigenome. J Mol Endocrinol 2008;41:91-102. https://doi.org/10.1677/JME-08-0025
  75. Sugino KY, Paneth N, Comstock SS. Michigan cohorts to determine associations of maternal pre-pregnancy body mass index with pregnancy and infant gastrointestinal microbial communities: late pregnancy and early infancy. PLoS One 2019;14:e0213733. https://doi.org/10.1371/journal.pone.0213733
  76. Mendez-Salazar EO, Ortiz-Lopez MG, Granados-Silvestre ML, Palacios-Gonzalez B, Menjivar M. Altered gut microbiota and compositional changes in firmicutes and proteobacteria in Mexican undernourished and obese children. Front Microbiol 2018;9:2494. https://doi.org/10.3389/fmicb.2018.02494
  77. Prescott SL, Wickens K, Westcott L, Jung W, Currie H, Black PN, et al. Supplementation with Lactobacillus rhamnosus or Bifidobacterium lactis probiotics in pregnancy increases cord blood interferon-gamma and breast milk transforming growth factor-beta and immunoglobin A detection. Clin Exp Allergy 2008;38:1606-1614. https://doi.org/10.1111/j.1365-2222.2008.03061.x