The relationship between early-life environment, the epigenome and the microbiota

Epigenomics

Volumn 7, Issue 7, 2015, Pages 1173-1184

  Majnik, Amber V ^a   Lane, Robert H ^a  

^a MEDICAL COLLEGE OF WISCONSIN   (United States)

Author keywords

early life adversity; environment; epigenetic; epigenome; histone modification; metabolite; methylation; microbiome

Indexed keywords

CHOLINE; DNA; FOLIC ACID; ISOTHIOCYANIC ACID DERIVATIVE; POLYPHENOL; SHORT CHAIN FATTY ACID; CHROMATIN; HISTONE; PROBIOTIC AGENT; VOLATILE FATTY ACID;

ARTICLE; CARBOHYDRATE DIET; DNA METHYLATION; ENVIRONMENTAL FACTOR; EPIGENETICS; GENE EXPRESSION; GENE INTERACTION; HUMAN; INTESTINE FLORA; MATERNAL NUTRITION; MICROBIAL COLONIZATION; MICROBIOME; MICROFLORA; NONHUMAN; PRIORITY JOURNAL; PROGENY; BIOSYNTHESIS; CHEMISTRY; CHROMATIN; DISEASE RESISTANCE; DRUG EFFECTS; GENETIC EPIGENESIS; GENETICS; GENOTYPE ENVIRONMENT INTERACTION; HUMAN GENOME; IMMUNOLOGY; METABOLISM; PHYSIOLOGY; PROTEIN PROCESSING;

CHOLINE; CHROMATIN; DISEASE RESISTANCE; DNA METHYLATION; EPIGENESIS, GENETIC; FATTY ACIDS, VOLATILE; FOLIC ACID; GENE-ENVIRONMENT INTERACTION; GENOME, HUMAN; HISTONES; HUMANS; ISOTHIOCYANATES; MICROBIOTA; POLYPHENOLS; PROBIOTICS; PROTEIN PROCESSING, POST-TRANSLATIONAL;

EID: 84949797048     PISSN: 17501911     EISSN: 1750192X     Source Type: Journal    
DOI: 10.2217/epi.15.74     Document Type: Article

References (125)

1. De Rooij SR, Painter RC, Phillips DI, et al. Hypothalamic-pituitary-adrenal axis activity in adults who were prenatally exposed to the dutch famine. Eur. J. Endocrinol. 155(1), 153-160 (2006
2. Roseboom TJ, Van Der Meulen JH, Osmond C, Barker DJ, Ravelli AC, Bleker OP. Plasma lipid profiles in adults after prenatal exposure to the dutch famine. Am. J. Clin. Nutr. 72(5), 1101-1106 (2000
3. Susser E, Neugebauer R, Hoek HW, et al. Schizophrenia after prenatal famine. Further evidence. Arch. Gen. Psychiatry 53(1), 25-31 (1996
4. Hughes LA, Van Den Brandt PA, De Bruine AP, et al. Early life exposure to famine and colorectal cancer risk: a role for epigenetic mechanisms. PLoS ONE 4(11), e7951 (2009
5. Russell SL, Gold MJ, Reynolds LA, et al. Perinatal antibiotic-induced shifts in gut microbiota have differential effects on inflammatory lung diseases. J. Allergy Clin. Immunol. 135(1), 100-109 (2015
6. Love C, David RJ, Rankin KM, Collins JW Jr. Exploring weathering: effects of lifelong economic environment and maternal age on low birth weight, small for gestational age, and preterm birth in African-American and white women. Am. J. Epidemiol. 172(2), 127-134 (2010
7. Tormo-Badia N, Hakansson A, Vasudevan K, Molin G, Ahrne S, Cilio CM. Antibiotic treatment of pregnant non-obese diabetic mice leads to altered gut microbiota and intestinal immunological changes in the offspring. Scand. J. Immunol. 80(4), 250-260 (2014
8. Hansen CH, Krych L, Buschard K, et al. A maternal glutenfree diet reduces inflammation and diabetes incidence in the offspring of nod mice. Diabetes 63(8), 2821-2832 (2014
9. Tobi EW, Lumey LH, Talens RP, et al. DNA methylation differences after exposure to prenatal famine are common and timing-and sex-specific. Hum. Mol. Genet. 18(21), 4046-4053 (2009
10. Heijmans BT, Tobi EW, Stein AD, et al. Persistent epigenetic differences associated with prenatal exposure to famine in humans. Proc. Natl Acad. Sci. USA 105(44), 17046-17049 (2008
11. Barrow TM, Michels KB. Epigenetic epidemiology of cancer. Biochem. Biophys. Res. Commun. 455(1-2), 70-83 (2014
12. Ogino S, Lochhead P, Chan AT, et al. Molecular pathological epidemiology of epigenetics: emerging integrative science to analyze environment, host, and disease. Mod. Pathol. 26(4), 465-484 (2013
13. Vickers MH. Early life nutrition, epigenetics and programming of later life disease. Nutrients 6(6), 2165-2178 (2014
14. Jimenez E, Fernandez L, Marin ML, et al. Isolation of commensal bacteria from umbilical cord blood of healthy neonates born by cesarean section. Curr. Microbiol. 51(4), 270-274 (2005
15. Dominguez-Bello MG, Costello EK, Contreras M, et al. Delivery mode shapes the acquisition and structure of the initial microbiota across multiple body habitats in newborns. Proc. Natl Acad. Sci. USA 107(26), 11971-11975 (2010
16. Ma J, Prince AL, Bader D, et al. High-fat maternal diet during pregnancy persistently alters the offspring microbiome in a primate model. Nat. Commun. 5, 3889 (2014
17. Human Microbiome Project Consortium. Structure, function and diversity of the healthy human microbiome. Nature 486(7402), 207-214 (2012
18. Wikoff WR, Anfora AT, Liu J, et al. Metabolomics analysis reveals large effects of gut microflora on mammalian blood metabolites. Proc. Natl Acad. Sci. USA 106(10), 3698-3703 (2009
19. Qin J, Li R, Raes J, et al. A human gut microbial gene catalogue established by metagenomic sequencing. Nature 464(7285), 59-65 (2010
20. Tremaroli V, Backhed F. Functional interactions between the gut microbiota and host metabolism. Nature 489(7415), 242-249 (2012
21. Nicholson JK, Holmes E, Kinross J, et al. Host-gut microbiota metabolic interactions. Science 336(6086), 1262-1267 (2012
22. Hill DA, Artis D. Intestinal bacteria and the regulation of immune cell homeostasis. Annu. Rev. Immunol. 28, 623-667 (2010
23. Round JL, Mazmanian SK. The gut microbiota shapes intestinal immune responses during health and disease. Nat. Rev. Immunol. 9(5), 313-323 (2009
24. Montiel-Castro AJ, Gonzalez-Cervantes RM, Bravo-Ruiseco G, Pacheco-Lopez G. The microbiota-gut-brain axis: neurobehavioral correlates, health and sociality. Front. Integr. Neurosci. 7, 70 (2013
25. Diaz Heijtz R, Wang S, Anuar F, et al. Normal gut microbiota modulates brain development and behavior. Proc. Natl Acad. Sci. USA 108(7), 3047-3052 (2011
26. Jimenez E, Marin ML, Martin R, et al. Is meconium from healthy newborns actually sterile? Res. Microbiol. 159(3), 187-193 (2008
27. Collado MC, Delgado S, Maldonado A, Rodriguez JM. Assessment of the bacterial diversity of breast milk of healthy women by quantitative real-time PCR. Lett. Appl. Microbiol. 48(5), 523-528 (2009
28. Aagaard K, Ma J, Antony KM, Ganu R, Petrosino J, Versalovic J. The placenta harbors a unique microbiome. Sci. Transl. Med. 6(237), 237ra265 (2014
29. Backhed F, Ding H, Wang T, et al. The gut microbiota as an environmental factor that regulates fat storage. Proc. Natl Acad. Sci. USA 101(44), 15718-15723 (2004
30. Turnbaugh PJ, Ridaura VK, Faith JJ, Rey FE, Knight R, Gordon JI. The effect of diet on the human gut microbiome: a metagenomic analysis in humanized gnotobiotic mice. Sci. Tansl. Med. 1(6), 6ra14 (2009
31. Salzman NH, Ghosh D, Huttner KM, Paterson Y, Bevins CL. Protection against enteric salmonellosis in transgenic mice expressing a human intestinal defensin. Nature 422(6931), 522-526 (2003
32. Morgan X, Kabakchiev B, Waldron L, et al. Associations between host gene expression, the mucosal microbiome, and clinical outcome in the pelvic pouch of patients with inflammatory bowel disease. Genome Biol. 16(1), 67 (2015
33. Knights D, Silverberg M, Weersma R, et al. Complex host genetics influence the microbiome in inflammatory bowel disease. Genome Med. 6(12), 107 (2014
34. Wen L, Ley RE, Volchkov PY, et al. Innate immunity and intestinal microbiota in the development of Type 1 diabetes. Nature 455(7216), 1109-1113 (2008
35. Myles IA, Fontecilla NM, Janelsins BM, Vithayathil PJ, Segre JA, Datta SK. Parental dietary fat intake alters offspring microbiome and immunity. J. Immunol. 191(6), 3200-3209 (2013
36. Alenghat T, Osborne LC, Saenz SA, et al. Histone deacetylase 3 coordinates commensal-bacteria-dependent intestinal homeostasis. Nature 504(7478), 153-157 (2013
37. Gao Z, Yin J, Zhang J, et al. Butyrate improves insulin sensitivity and increases energy expenditure in mice. Diabetes 58(7), 1509-1517 (2009
38. Kumar H, Lund R, Laiho A, et al. Gut microbiota as an epigenetic regulator: pilot study based on whole-genome methylation analysis. MBio 5(6), pii: e02113-14 (2014
39. Vaiserman A. Early-life origin of adult disease: evidence from natural experiments. Exp. Gerontol. 46(2-3), 189-192 (2011
40. Radford EJ, Ito M, Shi H, et al. In utero effects. In utero undernourishment perturbs the adult sperm methylome and intergenerational metabolism. Science 345(6198), 1255903 (2014
41. Ravelli AC, Van Der Meulen JH, Osmond C, Barker DJ, Bleker OP. Obesity at the age of 50 y in men and women exposed to famine prenatally. Am. J. Clin. Nutr. 70(5), 811-816 (1999
42. Van Abeelen AF, Elias SG, Bossuyt PM, et al. Famine exposure in the young and the risk of Type 2 diabetes in adulthood. Diabetes 61(9), 2255-2260 (2012
43. Ravelli AC, Van Der Meulen JH, Michels RP, et al. Glucose tolerance in adults after prenatal exposure to famine. Lancet 351(9097), 173-177 (1998
44. Roseboom TJ, Van Der Meulen JH, Osmond C, et al. Coronary heart disease after prenatal exposure to the dutch famine, 1944-45. Heart 84(6), 595-598 (2000
45. Hayward AD, Rickard IJ, Lummaa V. Influence of early-life nutrition on mortality and reproductive success during a subsequent famine in a preindustrial population. Proc. Natl Acad. Sci. USA 110(34), 13886-13891 (2013
46. Head R, Gilthorpe M, Byrom A, Ellison G. Cardiovascular disease in a cohort exposed to the 1940-45 channel islands occupation. BMC Public Health 8(1), 303 (2008
47. Neelsen S, Stratmann T. Effects of prenatal and early life malnutrition: evidence from the Greek famine. J. Health Econ. 30(3), 479-488 (2011
48. Roseboom TJ, Van Der Meulen JH, Ravelli AC, Osmond C, Barker DJ, Bleker OP. Perceived health of adults after prenatal exposure to the dutch famine. Paediatr. Perinat. Epidemiol. 17(4), 391-397 (2003
49. Roseboom TJ, Van Der Meulen JH, Osmond C, Barker DJ, Ravelli AC, Bleker OP. Adult survival after prenatal exposure to the Dutch famine 1944-45. Paediatr. Perinat. Epidemiol. 15(3), 220-225 (2001
50. Huang C, Li Z, Narayan KM, Williamson DF, Martorell, RL. Bigger babies born to women survivors of the 1959-1961 Chinese famine: a puzzle due to survival selection. J. Dev. Orig. Health Dis. 1(6), 1-7 (2010
51. Huang C, Li Z, Wang M, Martorell R. Early life exposure to the 1959-1961 Chinese famine has long-term health consequences. J. Nutr. 140(10), 1874-1878 (2010
52. Xiao X, Zhang ZX, Cohen HJ, et al. Evidence of a relationship between infant birth weight and later diabetes and impaired glucose regulation in a Chinese population. Diabetes Care 31(3), 483-487 (2008
53. Hult M, Tornhammar P, Ueda P, et al. Hypertension, diabetes and overweight: looming legacies of the Biafran famine. PLoS ONE 5(10), e13582 (2010
54. Van Der Sande MA, Coleman RL, Schim Van Der Loeff MF, et al. A template for improved prevention and control of cardiovascular disease in sub-saharan africa. Health Policy Plan. 16(4), 345-350 (2001
55. Musa DI, Toriola AL, Monyeki MA, Lawal B. Prevalence of childhood and adolescent overweight and obesity in Benue State, Nigeria. Trop. Med. Int. Health 17(11), 1369-1375 (2012
56. Oyeyemi AL, Adegoke BO, Oyeyemi AY, Deforche B, De Bourdeaudhuij I, Sallis JF. Environmental factors associated with overweight among adults in nigeria. Int. J. Behav. Nutr. Phys. Act. 9, 32 (2012
57. Huang C, Li Z, Venkat Narayan KM, Williamson DF, Martorell R. Bigger babies born to women survivors of the 1959-1961 Chinese famine: a puzzle due to survival selection? J. Dev. Orig. Health Dis. 1(06), 412-418 (2010
58. Fu Q, Yu X, Callaway CW, Lane RH, Mcknight RA. Epigenetics: intrauterine growth retardation (IUGR) modifies the histone code along the rat hepatic IGF-1 gene. FASEB J. 23(8), 2438-2449 (2009
59. Fu Q, Mcknight RA, Callaway CW, Yu X, Lane RH, Majnik AV. Intrauterine growth restriction disrupts developmental epigenetics around distal growth hormone response elements on the rat hepatic IGF-1 gene. FASEB J. 29(4), 1176-1184 (2014
60. Zhang S, Rattanatray L, Maclaughlin SM, et al. Periconceptional undernutrition in normal and overweight ewes leads to increased adrenal growth and epigenetic changes in adrenal IGF2/H19 gene in offspring. FASEB J. 24(8), 2772-2782 (2010
61. Sharif J, Nakamura M, Ito T, et al. Food restriction in pregnant mice can induce changes in histone modifications and suppress gene expression in fetus. Nucleic Acids Symp. Ser. (51), 125-126 (2007
62. Lillycrop KA, Phillips ES, Jackson AA, Hanson MA, Burdge GC. Dietary protein restriction of pregnant rats induces and folic acid supplementation prevents epigenetic modification of hepatic gene expression in the offspring. J. Nutr. 135(6), 1382-1386 (2005
63. Marco A, Kisliouk T, Tabachnik T, Meiri N, Weller A. Overweight and CpG methylation of the Pomc promoter in offspring of high-fat-diet-fed dams are not reprogrammed by regular chow diet in rats. FASEB J. 28(9), 4148-4157 (2014
64. Suter MA, Ma J, Vuguin PM, et al. In utero exposure to a maternal high-fat diet alters the epigenetic histone code in a murine model. Am. J. Obstet. Gynecol. 210(5), 463.e1-463.e11 (2014
65. Satokari R, Gronroos T, Laitinen K, Salminen S, Isolauri E. Bifidobacterium and Lactobacillus DNA in the human placenta. Lett. Appl. Microbiol. 48(1), 8-12 (2009
66. Digiulio DB, Romero R, Amogan HP, et al. Microbial prevalence, diversity and abundance in amniotic fluid during preterm labor: a molecular and culture-based investigation. PLoS ONE 3(8), e3056 (2008
67. Ardissone AN, De La Cruz DM, Davis-Richardson AG, et al. Meconium microbiome analysis identifies bacteria correlated with premature birth. PLoS ONE 9(3), e90784 (2014
68. Martin R, Heilig HG, Zoetendal EG, et al. Cultivationindependent assessment of the bacterial diversity of breast milk among healthy women. Res. Microbiol. 158(1), 31-37 (2007
69. Hunt KM, Foster JA, Forney LJ, et al. Characterization of the diversity and temporal stability of bacterial communities in human milk. PLoS ONE 6(6), e21313 (2011
70. Jost T, Lacroix C, Braegger CP, Rochat F, Chassard C. Vertical mother-neonate transfer of maternal gut bacteria via breastfeeding. Environ. Microbiol. 16(9), 2891-2904 (2014
71. Galley JD, Bailey M, Kamp Dush C, Schoppe-Sullivan S, Christian LM. Maternal obesity is associated with alterations in the gut microbiome in toddlers. PLoS ONE 9(11), e113026 (2014
72. Collado MC, Laitinen K, Salminen S, Isolauri E. Maternal weight and excessive weight gain during pregnancy modify the immunomodulatory potential of breast milk. Pediatr. Res. 72(1), 77-85 (2012
73. Sanz Y. Gut microbiota and probiotics in maternal and infant health. Am. J. Clin. Nutr. 94(Suppl. 6), s2000-s2005 (2011
74. Gueimonde M, Sakata S, Kalliomaki M, Isolauri E, Benno Y, Salminen S. Effect of maternal consumption of Lactobacillus GG on transfer and establishment of fecal bifidobacterial microbiota in neonates. J. Pediatr. Gastroenterol. Nutr. 42(2), 166-170 (2006
75. Schultz M, Gottl C, Young RJ, Iwen P, Vanderhoof JA. Administration of oral probiotic bacteria to pregnant women causes temporary infantile colonization. J. Pediatr. Gastroenterol. Nutr. 38(3), 293-297 (2004
76. Gronlund MM, Grzeskowiak L, Isolauri E, Salminen S. Influence of mother's intestinal microbiota on gut colonization in the infant. Gut Microbes 2(4), 227-233 (2011
77. Hallam MC, Barile D, Meyrand M, German JB, Reimer RA. Maternal high-protein or high-prebiotic-fiber diets affect maternal milk composition and gut microbiota in rat dams and their offspring. Obesity (Silver Spring) 22(11), 2344-2351 (2014
78. Schaible TD, Harris RA, Dowd SE, Smith CW, Kellermayer R. Maternal methyl-donor supplementation induces prolonged murine offspring colitis susceptibility in association with mucosal epigenetic and microbiomic changes. Hum. Mol. Genet. 20(9), 1687-1696 (2011
79. Mischke M, Plosch T. More than just a gut instinct-the potential interplay between a baby's nutrition, its gut microbiome, and the epigenome. Am. J. Physiol. Regul. Integr. Comp. Physiol. 304(12), R1065-R1069 (2013
80. Aufreiter S, Gregory JF, 3rd, Pfeiffer CM, et al. Folate is absorbed across the colon of adults: evidence from cecal infusion of (13)c-labeled [6s]-5-formyltetrahydrofolic acid. Am. J. Clin. Nutr. 90(1), 116-123 (2009
81. Okabe K, Hayashi M, Yoshida I, Nishimura K, Fukushima N, Tsujiuchi T. Distinct DNA methylation patterns of lysophosphatidic acid receptor genes during rat hepatocarcinogenesis induced by a choline-deficient l-amino acid-defined diet. Arch. Toxicol. 85(10), 1303-1310 (2011
82. Davison JM, Mellott TJ, Kovacheva VP, Blusztajn JK. Gestational choline supply regulates methylation of histone H3, expression of histone methyltransferases G9a (Kmt1c) and Suv39h1 (Kmt1a), and DNA methylation of their genes in rat fetal liver and brain. J. Biol. Chem. 284(4), 1982-1989 (2009
83. Lukovac S, Belzer C, Pellis L, et al. Differential modulation by Akkermansia muciniphila and Faecalibacterium prausnitzii of host peripheral lipid metabolism and histone acetylation in mouse gut organoids. MBio 5(4), e01438-14 (2014
84. Wong CP, Hsu A, Buchanan A, et al. Effects of sulforaphane and 3, 3′-diindolylmethane on genome-wide promoter methylation in normal prostate epithelial cells and prostate cancer cells. PLoS ONE 9(1), e86787 (2014
85. Liu Y, Chakravarty S, Dey M. Phenethylisothiocyanate alters site-and promoter-specific histone tail modifications in cancer cells. PLoS ONE 8(5), e64535 (2013
86. Izzotti A, Larghero P, Cartiglia C, et al. Modulation of microrna expression by budesonide, phenethyl isothiocyanate and cigarette smoke in mouse liver and lung. Carcinogenesis 31(5), 894-901 (2010
87. Kiss AK, Granica S, Stolarczyk M, Melzig MF. Epigenetic modulation of mechanisms involved in inflammation: influence of selected polyphenolic substances on histone acetylation state. Food Chem. 131(3), 1015-1020 (2012
88. Said HM, Mohammed ZM. Intestinal absorption of watersoluble vitamins: an update. Curr. Opin. Gastroenterol. 22(2), 140-146 (2006
89. Strozzi GP, Mogna L. Quantification of folic acid in human feces after administration of Bifidobacterium probiotic strains. J. Clin. Gastroenterol. 42(Suppl. 3 Pt 2), S179-S184 (2008
90. Pompei A, Cordisco L, Amaretti A, et al. Administration of folate-producing bifidobacteria enhances folate status in Wistar rats. J. Nutr. 137(12), 2742-2746 (2007
91. Wang Z, Klipfell E, Bennett BJ, et al. Gut flora metabolism of phosphatidylcholine promotes cardiovascular disease. Nature 472(7341), 57-63 (2011
92. Craciun S, Balskus EP. Microbial conversion of choline to trimethylamine requires a glycyl radical enzyme. Proc. Natl Acad. Sci. USA 109(52), 21307-21312 (2012
93. Thibodeaux CJ, Van Der Donk WA. Converging on a mechanism for choline degradation. Proc. Natl Acad. Sci. USA 109(52), 21184-21185 (2012
94. Corbin KD, Zeisel SH. Choline metabolism provides novel insights into nonalcoholic fatty liver disease and its progression. Curr. Opin. Gastroenterol. 28(2), 159-165 (2012
95. Okubo H, Sakoda H, Kushiyama A, et al. Lactobacillus casei strain shirota protects against nonalcoholic steatohepatitis development in a rodent model. Am. J. Physiol. Gastrointest. Liver Physiol. 305(12), G911-G918 (2013
96. Ishii D, Matsuzawa D, Matsuda S, Tomizawa H, Sutoh C, Shimizu E. Methyl donor-deficient diet during development can affect fear and anxiety in adulthood in C57BL/6J mice. PLoS ONE 9(8), e105750 (2014
97. Wong JM, De Souza R, Kendall CW, Emam A, Jenkins DJ. Colonic health: fermentation and short chain fatty acids. J. Clin. Gastroenterol. 40(3), 235-243 (2006
98. Den Besten G, Van Eunen K, Groen AK, Venema K, Reijngoud DJ, Bakker BM. The role of short-chain fatty acids in the interplay between diet, gut microbiota, and host energy metabolism. J. Lipid Res. 54(9), 2325-2340 (2013
99. Riggs MG, Whittaker RG, Neumann JR, Ingram VM. N-butyrate causes histone modification in HeLa and Friend erythroleukaemia cells. Nature 268(5619), 462-464 (1977
100. Candido EP, Reeves R, Davie JR. Sodium butyrate inhibits histone deacetylation in cultured cells. Cell 14(1), 105-113 (1978
101. Sealy L, Chalkley R. The effect of sodium butyrate on histone modification. Cell 14(1), 115-121 (1978
102. Boffa LC, Vidali G, Mann RS, Allfrey VG. Suppression of histone deacetylation in vivo and in vitro by sodium butyrate. J. Biol. Chem. 253(10), 3364-3366 (1978
103. Vidali G, Boffa LC, Bradbury EM, Allfrey VG. Butyrate suppression of histone deacetylation leads to accumulation of multiacetylated forms of histones H3 and H4 and increased DNase I sensitivity of the associated DNA sequences. Proc. Natl Acad. Sci. USA 75(5), 2239-2243 (1978
104. Lenzi M, Fimognari C, Hrelia P. Sulforaphane as a promising molecule for fighting cancer. Cancer Treat. Res. 159, 207-223 (2014
105. Gupta P, Wright SE, Kim SH, Srivastava SK. Phenethyl isothiocyanate: a comprehensive review of anti-cancer mechanisms. Biochim. Biophys. Acta 1846(2), 405-424 (2014
106. Choi KM, Lee YS, Sin DM, et al. Sulforaphane inhibits mitotic clonal expansion during adipogenesis through cell cycle arrest. Obesity (Silver Spring) 20(7), 1365-1371 (2012
107. Kim SH, Nagalingam A, Saxena NK, Singh SV, Sharma D. Benzyl isothiocyanate inhibits oncogenic actions of leptin in human breast cancer cells by suppressing activation of signal transducer and activator of transcription 3. Carcinogenesis 32(3), 359-367 (2011
108. Yuan GF, Sun B, Yuan J, Wang QM. Effects of different cooking methods on health-promoting compounds of broccoli. J. Zhejiang Univ. Sci. B 10(8), 580-588 (2009
109. Brabban AD, Edwards C. Isolation of glucosinolate degrading microorganisms and their potential for reducing the glucosinolate content of rapemeal. FEMS Microbiol. Lett. 119(1-2), 83-88 (1994
110. Elfoul L, Rabot S, Khelifa N, Quinsac A, Duguay A, Rimbault A. Formation of allyl isothiocyanate from sinigrin in the digestive tract of rats monoassociated with a human colonic strain of Bacteroides thetaiotaomicron. FEMS Microbiol. Lett. 197(1), 99-103 (2001
111. Yang P, He X, Malhotra A. Epigenetic targets of polyphenols in cancer. J. Environ. Pathol. Toxicol. Oncol. 33(2), 159-165 (2014
112. Yamagata K, Tagami M, Yamori Y. Dietary polyphenols regulate endothelial function and prevent cardiovascular disease. Nutrition 31(1), 28-37 (2015
113. Carpene C, Gomez-Zorita S, Deleruyelle S, Carpene MA. Novel strategies for preventing diabetes and obesity complications with natural polyphenols. Curr. Med. Chem. 22(1), 150-164 (2015
114. Wang S, Moustaid-Moussa N, Chen L, et al. Novel insights of dietary polyphenols and obesity. J. Nutr. Biochem. 25(1), 1-18 (2014
115. Marin L, Miguelez EM, Villar CJ, Lombo F. Bioavailability of dietary polyphenols and gut microbiota metabolism: antimicrobial properties. Biomed. Res. Int. 2015, 905215 (2015
116. Duenas M, Munoz-Gonzalez I, Cueva C, et al. A survey of modulation of gut microbiota by dietary polyphenols. Biomed. Res. Int. 2015, 850902 (2015
117. Cerda B, Espin JC, Parra S, Martinez P, Tomas-Barberan FA. The potent in vitro antioxidant ellagitannins from pomegranate juice are metabolised into bioavailable but poor antioxidant hydroxy-6h-dibenzopyran-6-one derivatives by the colonic microflora of healthy humans. Eur. J. Nutr. 43(4), 205-220 (2004
118. Ito H. Metabolites of the ellagitannin geraniin and their antioxidant activities. Planta Med. 77(11), 1110-1115 (2011
119. Reddy MK, Gupta SK, Jacob MR, Khan SI, Ferreira D. Antioxidant, antimalarial and antimicrobial activities of tannin-rich fractions, ellagitannins and phenolic acids from punica granatum l. Planta Med. 73(5), 461-467 (2007
120. Wang CC, Chen LG, Yang LL. Antitumor activity of four macrocyclic ellagitannins from cuphea hyssopifolia. Cancer Lett. 140(1-2), 195-200 (1999
121. Lipinska L, Klewicka E, Sojka M. The structure, occurrence and biological activity of ellagitannins: a general review. Acta Sci. Pol. Technol. Aliment. 13(3), 289-299 (2014
122. Sangiovanni E, Vrhovsek U, Rossoni G, et al. Ellagitannins from rubus berries for the control of gastric inflammation: in vitro and in vivo studies. PLoS ONE 8(8), e71762 (2013
123. Zou X, Yan C, Shi Y, et al. Mitochondrial dysfunction in obesity-associated nonalcoholic fatty liver disease: the protective effects of pomegranate with its active component punicalagin. Antioxid. Redox Signal. 21(11), 1557-1570 (2014
124. Ghadimi D, Helwig U, Schrezenmeir J, Heller KJ, De Vrese M. Epigenetic imprinting by commensal probiotics inhibits the IL-23/IL-17 axis in an in vitro model of the intestinal mucosal immune system. J. Leukoc. Biol. 92(4), 895-911 (2012
125. Donohoe DR, Holley D, Collins LB, et al. A gnotobiotic mouse model demonstrates that dietary fiber protects against colorectal tumorigenesis in a microbiota-and butyratedependent manner. Cancer Discov. 4(12), 1387-1397 (2014