Epigenetic Regulation of Gastrointestinal Epithelial Barrier and Developmental Origins of Health and Disease

The Epigenome and Developmental Origins of Health and Disease

Volumn , Issue , 2015, Pages 337-360

  Lalles J P ^a,b   Michel, C ^b,c,d   Theodorou, V ^a   Segain, J P ^b,c,d  

^a CEMAGREF   (France)

^b Centre de Recherche en Nutrition HumaineOuest   (France)

^c Universite de Nantes   (France)

^d Institut des Maladies de l'Appareil Digestif   (France)

Author keywords

Cancer; Colon; Developmental origin of health and disease; Epigenetics; Epithelial barrier; Inflammation; Intestine; Microbiota; Programming; Stress

Indexed keywords

EID: 84977442848     PISSN: None     EISSN: None     Source Type: Book    
DOI: 10.1016/B978-0-12-801383-0.00017-7     Document Type: Chapter

References (196)

1. Turner J.R. Intestinal mucosal barrier function in health and disease. Nat Rev Immunol 2009, 9:799-809.
2. Huang X.Z., Zhu L.B., Li Z.R., Lin J. Bacterial colonization and intestinal mucosal barrier development. World J Clin Pediatr 2013, 2:46-53.
3. Pastorelli L., De Salvo C., Mercado J.R., Vecchi M., Pizarro T.T. Central role of the gut epithelial barrier in the pathogenesis of chronic intestinal inflammation: lessons learned from animal models and human genetics. Front Immunol 2013, 4:280.
4. Shanahan F., Quigley E.M. Manipulation of the microbiota for treatment of IBS and IBD-challenges and controversies. Gastroenterology 2014, 146:1554-1563.
5. Katiraei P., Gilberto Bultron G. Need for a comprehensive medical approach to the neuroimmuno-gastroenterology of irritable bowel syndrome. World J Gastroenterol 2011, 17:2791-2800.
6. Viaud S., Daillère R., Boneca I.G., Lepage P., Pittet M.J., Ghiringhelli F., et al. Harnessing the intestinal microbiome for optimal therapeutic immunomodulation. Cancer Res 2014, 74:4217-4221.
7. Burisch J., Jess T., Martinato M., Lakatos P.L., ECCO -EpiCom The burden of inflammatory bowel disease in Europe. J Crohns Colitis 2013, 7(4):322-337.
8. Herszényi L., Barabás L., Miheller P., Tulassay Z. Colorectal cancer in patients with inflammatory bowel disease: the true impact of the risk. Dig Dis 2015, 33(1):52-57.
9. Hungin A.P., Chang L., Locke G.R., Dennis E.H., Barghout V. Irritable bowel syndrome in the United States: prevalence, symptom patterns and impact. Aliment Pharmacol Ther 2005, 21:1365-1375.
10. Brenner H., Kloor M., Pox C.P. Colorectal cancer. Lancet 2014, 383(9927):1490-1502.
11. Renz H., von Mutius E., Brandtzaeg P., Cookson W.O., Autenrieth I.B., Haller D. Gene-environment interactions in chronic inflammatory disease. Nat Immunol 2011, 12:273-277.
12. Vaiopoulou A., Karamanolis G., Psaltopoulou T., Karatzias G., Gazouli M. Molecular basis of the irritable bowel syndrome. World J Gastroenterol 2014, 20:376-383.
13. Arasaradnam R.P., Commane D.M., Bradburn D., Mathers J.C. A review of dietary factors and its influence on DNA methylation in colorectal carcinogenesis. Epigenetics 2008, 3:193-198.
14. Jaenisch R., Bird A. Epigenetic regulation of gene expression: how the genome integrates intrinsic and environmental signals. Nat Genet 2003, (33 Suppl.):245-254.
15. Feil R., Fraga M.F. Epigenetics and the environment: emerging patterns and implications. Nat Rev Genet 2012, 13:97-109.
16. Nian H., Delage B., Ho E., Dashwood R.H. Modulation of histone deacetylase activity by dietary isothiocyanates and allyl sulfides: studies with sulforaphane and garlic organosulfur compounds. Environ Mol Mutagen 2009, 50:213-221.
17. Lallès J.P. Long term effects of pre- and early postnatal nutrition and environment on the gut. J Anim Sci 2012, 90(Suppl. 4):421-429.
18. Wall R., Ross R.P., Ryan C.A., Hussey S., Murphy B., Fitzgerald G.F., et al. Role of gut microbiota in early infant development. Clin Med Pediatr 2009, 3:45-54.
19. Canani R.B., Costanzo M.D., Leone L., Bedogni G., Brambilla P., Cianfarani S., et al. Epigenetic mechanisms elicited by nutrition in early life. Nutr Res Rev 2011, 24:198-205.
20. Morel F.B., Oozeer R., Piloquet H., Moyon T., Pagniez A., Knol J., Darmaun D., et al. Preweaning modulation of intestinal microbiota by oligosaccharides or amoxicillin can contribute to programming of adult microbiota in rats. Nutrition 2015, 31:515-522.
21. Haemer M.A., Huang T.T., Daniels S.R. The effect of neurohormonal factors, epigenetic factors, and gut microbiota on risk of obesity. Prev Chronic Dis 2009, 6:A96.
22. Reinhardt C., Reigstad C.S., Backhed F. Intestinal microbiota during infancy and its implications for obesity. J Pediatr Gastroenterol Nutr 2009, 48:249-256.
23. Backhed F. Programming of host metabolism by the gut microbiota. Ann Nutr Metab 2011, 58(Suppl. 2):44-52.
24. Kaplan J.L., Walker W.A. Early gut colonization and subsequent obesity risk. Curr Opin Clin Nutr Metab Care 2012, 15:278-284.
25. Kellermayer R. Epigenetics and the developmental origins of inflammatory bowel diseases. Can J Gastroenterol 2012, 26:909-915.
26. Shenderov B.A. Gut indigenous microbiota and epigenetics. Microb Ecol Health Dis 2012, 23.
27. 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 2013, 304:R1065-R1069.
28. Shenderov B.A., Midtvedt T. Epigenomic programing: a future way to health?. Microb Ecol Health Dis 2014, 25.
29. Takahashi K. Influence of bacteria on epigenetic gene control. Cell Mol Life Sci 2014, 71:1045-1054.
30. Mackie R.I., Sghir A., Gaskins H.R. Developmental microbial ecology of the neonatal gastrointestinal tract. Am J Clin Nutr 1999, 69:1035S-1045S.
31. Yatsunenko T., Rey F.E., Manary M.J., Trehan I., Dominguez-Bello M.G., Contreras M., et al. Human gut microbiome viewed across age and geography. Nature 2012, 486:222-227.
32. Crott J.W., Liu Z., Keyes M.K., Choi S.W., Jang H., Moyer M.P., et al. Moderate folate depletion modulates the expression of selected genes involved in cell cycle, intracellular signaling and folate uptake in human colonic epithelial cell lines. J Nutr Biochem 2008, 19:328-335.
33. Mariadason J.M., Corner G.A., Augenlicht L.H. Genetic reprogramming in pathways of colonic cell maturation induced by short chain fatty acids: comparison with trichostatin A, sulindac, and curcumin and implications for chemoprevention of colon cancer. Cancer Res 2000, 60:4561-4572.
34. Donohoe D.R., Collins L.B., Wali A., Bigler R., Sun W., Bultman S.J. The Warburg effect dictates the mechanism of butyrate-mediated histone acetylation and cell proliferation. Mol Cell 2012, 48:612-626.
35. Choi S.W., Friso S. Epigenetics: a new bridge between nutrition and health. Adv Nutr 2010, 1:8-16.
36. Donohoe D.R., Bultman S.J. Metaboloepigenetics: interrelationships between energy metabolism and epigenetic control of gene expression. J Cell Physiol 2012, 227:3169-3177.
37. McKay J.A., Mathers J.C. Diet induced epigenetic changes and their implications for health. Acta Physiol (Oxf) 2011, 202:103-118.
38. Anderson O.S., Sant K.E., Dolinoy D.C. Nutrition and epigenetics: an interplay of dietary methyl donors, one-carbon metabolism and DNA methylation. J Nutr Biochem 2012, 23:853-859.
39. Johnson I.T., Belshaw N.J. The effect of diet on the intestinal epigenome. Epigenomics 2014, 6:239-251.
40. Waterland R.A., Jirtle R.L. Transposable elements: targets for early nutritional effects on epigenetic gene regulation. Mol Cell Biol 2003, 23:5293-5300.
41. Heijmans B.T., Tobi E.W., Stein A.D., Putter H., Blauw G.J., Susser E.S., et al. Persistent epigenetic differences associated with prenatal exposure to famine in humans. Proc Natl Acad Sci USA 2008, 105:17046-17049.
42. Joss-Moore L.A., Lane R.H. The developmental origins of adult disease. Curr Opin Pediatr 2009, 21:230-234.
43. Vincent A., Van Seuningen I. Epigenetics, stem cells and epithelial cell fate. Differentiation 2009, 78:99-107.
44. Spivakov M., Fisher A.G. Epigenetic signatures of stem-cell identity. Nat Rev Genet 2007, 8:263-271.
45. van der Flier L.G., Clevers H. Stem cells, self-renewal, and differentiation in the intestinal epithelium. Annu Rev Physiol 2009, 71:241-260.
46. Nadauld L.D., Phelps R., Moore B.C., Eisinger A., Sandoval I.T., Chidester S., et al. Adenomatous polyposis coli control of C-terminal binding protein-1 stability regulates expression of intestinal retinol dehydrogenases. J Biol Chem 2006, 281:37828-37835.
47. Rai K., Sarkar S., Broadbent T.J., Voas M., Grossmann K.F., Nadauld L.D., et al. DNA demethylase activity maintains intestinal cells in an undifferentiated state following loss of APC. Cell 2010, 142:930-942.
48. Hammoud S.S., Cairns B.R., Jones D.A. Epigenetic regulation of colon cancer and intestinal stem cells. Curr Opin Cell Biol 2013, 25:177-183.
49. Azuara V., Perry P., Sauer S., Spivakov M., Jørgensen H.F., John R.M., et al. Chromatin signatures of pluripotent cell lines. Nat Cell Biol 2006, 8:532-538.
50. Bernstein B.E., Mikkelsen T.S., Xie X., Kamal M., Huebert D.J., Cuff J., et al. A bivalent chromatin structure marks key developmental genes in embryonic stem cells. Cell 2006, 125:315-326.
51. Benoit Y.D., Lepage M.B., Khalfaoui T., Tremblay E., Basora N., Carrier J.C., et al. Polycomb repressive complex 2 impedes intestinal cell terminal differentiation. J Cell Sci 2012, 125:3454-3463.
52. Wilson A.J., Byun D.S., Popova N., Murray L.B., L'Italien K., Sowa Y., et al. Histone deacetylase 3 (HDAC3) and other class I HDACs regulate colon cell maturation and p21 expression and are deregulated in human colon cancer. J Biol Chem 2006, 281:13548-13558.
53. Tou L., Liu Q., Shivdasani R.A. Regulation of mammalian epithelial differentiation and intestine development by class I histone deacetylases. Mol Cell Biol 2004, 24:3132-3139.
54. de Rooij S.R., Roseboom T.J. The developmental origins of ageing: study protocol for the Dutch famine birth cohort study on ageing. BMJ Open 2013, 3:e003167.
55. Steegenga W.T., de Wit N.J., Boekschoten M.V., Ijssennagger N., Lute C., Keshtkar S., et al. Structural, functional and molecular analysis of the effects of aging in the small intestine and colon of C57BL/6J mice. BMC Med Genomics 2012, 5:38.
56. Steine E.J., Ehrich M., Bell G.W., Raj A., Reddy S., van Oudenaarden A., et al. Genes methylated by DNA methyltransferase 3b are similar in mouse intestine and human colon cancer. J Clin Invest 2011, 121:1748-1752.
57. McKay J.A., Waltham K.J., Williams E.A., Mathers J.C. Folate depletion during pregnancy and lactation reduces genomic DNA methylation in murine adult offspring. Genes Nutr 2011, 6:189-196.
58. McKay J.A., Williams E.A., Mathers J.C. Effect of maternal and post-weaning folate supply on gene-specific DNA methylation in the small intestine of weaning and adult apc and wild type mice. Front Genet 2011, 2:23.
59. Schaible T.D., Harris R.A., Dowd S.E., Smith C.W., Kellermayer R. Maternal methyl-donor supplementation induces prolonged murine offspring colitis susceptibility in association with mucosal epigenetic and microbiomic changes. Hum Mol Genet 2011, 20:1687-1696.
60. Mir S.A., Nagy-Szakal D., Dowd S.E., Szigeti R.G., Smith C.W., Kellermayer R. Prenatal methyl-donor supplementation augments colitis in young adult mice. PLoS One 2013, 8:e73162.
61. Blottière H.M., de Vos W.M., Ehrlich S.D., Doré J. Human intestinal metagenomics: state of the art and future. Curr Opin Microbiol 2013, 16:232-239.
62. Lepage P., Leclerc M.C., Joossens M., Mondot S., Blottière H.M., Raes J., et al. A metagenomic insight into our gut's microbiome. Gut 2013, 62:146-158.
63. Doré J., Corthier G. The human intestinal microbia. Gastroentérol Clin Biol 2010, 34:7-16.
64. Bäckhed F., Ley R.E., Sonnenburg J.L., Peterson D.A., Gordon J.I. Host-bacterial mutualism in the human intestine. Science 2005, 307:1915-1920.
65. Tap J., Mondot S., Levenez F., Pelletier E., Caron C., Furet J.P., et al. Towards the human intestinal microbiota phylogenetic core. Environ Microbiol 2009, 11:2574-2584.
66. Li J., Jia H., Cai X., Zhong H., Feng Q., Sunagawa S., et al. An integrated catalog of reference genes in the human gut microbiome. Nat Biotechnol 2014, 32:834-841. MetaHIT Consortium.
67. Qin J., Li R., Raes J., Arumugam M., Arumugam M., Burgdorf K.S., et al. A human gut microbial gene catalogue established by metagenomic sequencing. Nature 2010, 464:59-65. MetaHIT Consortium.
68. Kurokawa K., Itoh T., Kuwahara T., Oshima K., Toh H., Toyoda A., et al. Comparative metagenomics revealed commonly enriched gene sets in human gut microbiomes. DNA Res 2007, 14:169-181.
69. Arumugam M., Raes J., Pelletier E., Le Paslier D., Yamada T., Mende D.R., et al. Enterotypes of the human gut microbiome. Nature 2011, 473:174-180. MetaHIT Consortium.
70. Possemiers S., Bolca S., Verstraete W., Heyerick A. The intestinal microbiome: a separate organ inside the body with the metabolic potential to influence the bioactivity of botanicals. Fitoterapia 2011, 82:53-66.
71. Sekirov I., Russell S.L., Antunes L.C., Finlay B.B. Gut microbiota in health and disease. Physiol Rev 2010, 90:859-904.
72. Macfarlane G.T., Macfarlane S. Bacteria, colonic fermentation, and gastrointestinal health. J AOAC Int 2012, 95:50-60.
73. Sayin S.I., Wahlström A., Felin J., Jäntti S., Marschall H.U., Bamberg K., et al. Gut microbiota regulates bile acid metabolism by reducing the levels of tauro-beta-muricholic acid, a naturally occurring FXR antagonist. Cell Metab 2013, 17:225-235.
74. Wang Z., Klipfell E., Bennett B.J., Koeth R., Levison B.S., Dugar B., et al. Gut flora metabolism of phosphatidylcholine promotes cardiovascular disease. Nature 2011, 472:57-63.
75. Gérard P., Béguet F., Lepercq P., Rigottier-Gois L., Rochet V., Andrieux C., et al. Gnotobiotic rats harboring human intestinal microbiota as a model for studying cholesterol-to-coprostanol conversion. FEMS Microbiol Ecol 2004, 47:337-343.
76. Hill M.J. Intestinal flora and endogenous vitamin synthesis. Eur J Cancer Prev 1997, 6(Suppl. 1):S43-S45.
77. Krul C., Humblot C., Philippe C., Vermeulen M., van Nuenen M., Havenaar R., et al. Metabolism of sinigrin (2-propenyl glucosinolate) by the human colonic microflora in a dynamic in vitro large-intestinal model. Carcinogenesis 2002, 23:1009-1016.
78. Wikoff W.R., Anfora A.T., Liu J., Schultz P.G., Lesley S.A., Peters E.C., et al. Metabolomics analysis reveals large effects of gut microflora on mammalian blood metabolites. Proc Natl Acad Sci USA 2009, 106:3698-3703.
79. Rezzonico E., Mestdagh R., Delley M., Combremont S., Dumas M.E., Holmes E., et al. Bacterial adaptation to the gut environment favors successful colonization: microbial and metabonomic characterization of a simplified microbiota mouse model. Gut Microbes 2011, 2:307-318.
80. Bierne H., Hamon M., Cossart P. Epigenetics and bacterial infections. Cold Spring Harb Perspect Med 2012, 2:a010272.
81. Al Akeel R. Role of epigenetic reprogramming of host genes in bacterial pathogenesis. Saudi J Biol Sci 2013, 20:305-309.
82. Niwa T., Tsukamoto T., Toyoda T., Mori A., Tanaka H., Maekita T., et al. Inflammatory processes triggered by Helicobacter pylori infection cause aberrant DNA methylation in gastric epithelial cells. Cancer Res 2010, 70:1430-1440.
83. Boffa L.C., Vidali G., Mann R.S., Allfrey V.G. Suppression of histone deacetylation in vivo and in vitro by sodium butyrate. J Biol Chem 1978, 253:3364-3366.
84. LeBlanc J.G., Milani C., de Giori G.S., Sesma F., van Sinderen D., Ventura M. Bacteria as vitamin suppliers to their host: a gut microbiota perspective. Curr Opin Biotechnol 2013, 24:160-168.
85. Kim G.W., Gocevski G., Wu C.J., Yang X.J. Dietary, metabolic, and potentially environmental modulation of the lysine acetylation machinery. Int J Cell Biol 2010, 2010:632739.
86. Pessione E. Lactic acid bacteria contribution to gut microbiota complexity: lights and shadows. Front Cell Infect Microbiol 2012, 2:86.
87. Hrdina J., Banning A., Kipp A., Loh G., Blaut M., Brigelius-Flohé R. The gastrointestinal microbiota affects the selenium status and selenoprotein expression in mice. J Nutr Biochem 2009, 20:638-648.
88. Barrera L.N., Cassidy A., Johnson I.T., Bao Y., Belshaw N.J. Epigenetic and antioxidant effects of dietary isothiocyanates and selenium: potential implications for cancer chemoprevention. Proc Nutr Soc 2012, 71:237-245.
89. Alenghat T., Osborne L.C., Saenz S.A., Kobuley D., Ziegler C.G., Mullican S.E., et al. Histone deacetylase 3 coordinates commensal-bacteria-dependent intestinal homeostasis. Nature 2013, 504:153-157.
90. Takahashi K., Sugi Y., Nakano K., Tsuda M., Kurihara K., Hosono A., et al. Epigenetic control of the host gene by commensal bacteria in large intestinal epithelial cells. J Biol Chem 2011, 286:35755-35762.
91. Olszak T., An D., Zeissig S., Vera M.P., Richter J., Franke A., et al. Microbial exposure during early life has persistent effects on natural killer T cell function. Science 2012, 336:489-493.
92. Burcelin R., Serino M., Chabo C., Blasco-Baque V., Amar J. Gut microbiota and diabetes: from pathogenesis to therapeutic perspective. Acta Diabetol 2011, 48:257-273.
93. Marques T.M., Wall R., Ross R.P., Fitzgerald G.F., Ryan C.A., Stanton C. Programming infant gut microbiota: influence of dietary and environmental factors. Curr Opin Biotechnol 2010, 21:149-156.
94. Fujiwara R., Takemura N., Watanabe J., Sonoyama K. Maternal consumption of fructo-oligosaccharide diminishes the severity of skin inflammation in offspring of NC/Nga mice. Br J Nutr 2010, 103:530-538.
95. Ellis-Pegler R.B., Crabtree C., Lambert H.P. The faecal flora of children in the United Kingdom. J Hyg (Lond) 1975, 75:135-142.
96. Tannock G.W. What immunologists should know about bacterial communities of the human bowel. Semin Immunol 2007, 19:94-105.
97. Inoue R., Ushida K. Development of the intestinal microbiota in rats and its possible interactions with the evolution of the luminal IgA in the intestine. FEMS Microbiol Ecol 2003, 45:147-153.
98. Fança-Berthon P., Hoebler C., Mouzet E., David A., Michel C. Intrauterine growth restriction not only modifies the cecocolonic microbiota in neonatal rats but also affects its activity in young adult rats. J Pediatr Gastroenterol Nutr 2010, 51:402-413.
99. Rinne M., Kalliomaki M., Salminen S., Isolauri E. Probiotic intervention in the first months of life: short-term effects on gastrointestinal symptoms and long-term effects on gut microbiota. J Pediatr Gastroenterol Nutr 2006, 43:200-205.
100. Salvini F., Riva E., Salvatici E., Boehm G., Jelinek J., Banderali G., et al. A specific prebiotic mixture added to starting infant formula has long-lasting bifidogenic effects. J Nutr 2011, 141:1335-1339.
101. Gronlund M.M., Lehtonen O.P., Eerola E., Kero P. Fecal microflora in healthy infants born by different methods of delivery: permanent changes in intestinal flora after cesarean delivery. J Pediatr Gastroenterol Nutr 1999, 28:19-25.
102. Salminen S., Gibson G.R., McCartney A.L., Isolauri E. Influence of mode of delivery on gut microbiota composition in seven year old children. Gut 2004, 53:1388-1389.
103. Eggesbø M., Moen B., Peddada S., Baird D., Rugtveit J., Midtvedt T., et al. Development of gut microbiota in infants not exposed to medical interventions. APMIS 2011, 119:17-35.
104. Scholtens P.A., Oozeer R., Martin R., Amor K.B., Knol J. The early settlers: intestinal microbiology in early life. Annu Rev Food Sci Technol 2012, 3:425-447.
105. Roediger W.E. Utilization of nutrients by isolated epithelial cells of the rat colon. Gastroenterology 1982, 83:424-429.
106. Davie J.R. Inhibition of histone deacetylase activity by butyrate. J Nutr 2003, 133:2485S-2493S.
107. Donohoe D.R., Garge N., Zhang X., Sun W., O'Connell T.M., Bunger M.K., et al. The microbiome and butyrate regulate energy metabolism and autophagy in the mammalian colon. Cell Metab 2011, 13:517-526.
108. Hinnebusch B.F., Meng S., Wu J.T., Archer S.Y., Hodin R.A. The effects of short-chain fatty acids on human colon cancer cell phenotype are associated with histone hyperacetylation. J Nutr 2002, 132:1012-1017.
109. Hinnebusch B.F., Henderson J.W., Siddique A., Malo M.S., Zhang W., Abedrapo M.A., et al. Transcriptional activation of the enterocyte differentiation marker intestinal alkaline phosphatase is associated with changes in the acetylation state of histone H3 at a specific site within its promoter region in vitro. J Gastrointest Surg 2003, 7:237-244. Discussion 244-5.
110. Shin J., Carr A., Corner G.A., Tögel L., Dávaos-Salas M., Tran H., et al. The intestinal epithelial cell differentiation marker intestinal alkaline phosphatase (ALPi) is selectively induced by histone deacetylase inhibitors (HDACi) in colon cancer cells in a Kruppel-like factor 5 (KLF5)-dependent manner. J Biol Chem 2014, 289:25306-25316.
111. Lallès J.P. Intestinal alkaline phosphatase: multiple biological roles in maintenance of intestinal homeostasis and modulation by diet. Nutr Rev 2010, 68:323-332.
112. Lallès J.P. Intestinal alkaline phosphatase: novel functions and protective effects. Nutr Rev 2014, 72:82-94.
113. Malo M.S., Moaven O., Muhammad N., Biswas B., Alam S.N., Economopoulos K.P., et al. Intestinal alkaline phosphatase promotes gut bacterial growth by reducing the concentration of luminal nucleotide triphosphates. Am J Physiol Gastrointest Liver Physiol 2014, 306:G826-G838.
114. Cani P.D., Delzenne N.M. The role of the gut microbiota in energy metabolism and metabolic disease. Curr Pharm Des 2009, 15:1546-1558.
115. Arnal M.E., Zhang J., Messori S., Bosi P., Smidt H., Lallès J.P. Early changes in microbial colonization selectively modulate intestinal enzymes, but not inducible heat shock proteins in young adult Swine. PLoS One 2014, 9:e87967. Erratum in: PLoS One 2014;9:e98730.
116. Waterland R.A. Epigenetic mechanisms and gastrointestinal development. J Pediatr 2006, 149:S137-S142.
117. Thibault R., Blachier F., Darcy-Vrillon B., de Coppet P., Bourreille A., Segain J.P. Butyrate utilization by the colonic mucosa in inflammatory bowel diseases: a transport deficiency. Inflamm Bowel Dis 2010, 16:684-695.
118. Rodríguez-Paredes M., Esteller M. Cancer epigenetics reaches mainstream oncology. Nat Med 2011, 17:330-339.
119. Toyota M., Ahuja N., Ohe-Toyota M., Herman J.G., Baylin S.B., Issa J.P. CpG island methylator phenotype in colorectal cancer. Proc Natl Acad Sci USA 1999, 96:8681-8686.
120. Huttenhower C., Kostic A.D., Xavier R.J. Inflammatory bowel disease as a model for translating the microbiome. Immunity 2014, 40:843-854.
121. Sonntag B., Stolze B., Heinecke A., Luegering A., Heidemann J., Lebiedz P., et al. Preterm birth but not mode of delivery is associated with an increased risk of developing inflammatory bowel disease later in life. Inflamm Bowel Dis 2007, 13:1385-1390.
122. Corrao G., Tragnone A., Caprilli R., Trallori G., Papi C., Andreoli A., et al. Risk of inflammatory bowel disease attributable to smoking, oral contraception and breastfeeding in Italy: a nationwide case-control study. Cooperative Investigators of the Italian Group for the Study of the Colon and the Rectum (GISC). Int J Epidemiol 1998, 27:397-404.
123. Ekbom A., Adami H.O., Helmick C.G., Jonzon A., Zack M.M. Perinatal risk factors for inflammatory bowel disease: a case-control study. Am J Epidemiol 1990, 132:1111-1119.
124. Klement E., Cohen R.V., Boxman J., Joseph A., Reif S. Breastfeeding and risk of inflammatory bowel disease: a systematic review with meta-analysis. Am J Clin Nutr 2004, 80:1342-1352.
125. Khalili H., Ananthakrishnan A.N., Higuchi L.M., Richter J.M., Fuchs C.S., Chan A.T. Early life factors and risk of inflammatory bowel disease in adulthood. Inflamm Bowel Dis 2013, 19:542-547.
126. Fança-Berthon P., Michel C., Pagniez A., Rival M., Van Seuningen I., Darmaun D., et al. Intrauterine growth restriction alters postnatal colonic barrier maturation in rats. Pediatr Res 2009, 66:47-52.
127. Le Dréan G., Haure-Mirande V., Ferrier L., Bonnet C., Hulin P., de Coppet P., et al. Visceral adipose tissue and leptin increase colonic epithelial tight junction permeability via a RhoA-ROCK-dependent pathway. FASEB J 2014, 28:1059-1070.
128. Lallès J.P., Orozco-Solís R., Bolaños-Jiménez F., de Coppet P., Le Dréan G., Segain J.P. Perinatal undernutrition alters intestinal alkaline phosphatase and its main transcription factors KLF4 and Cdx1 in adult offspring fed a high-fat diet. J Nutr Biochem 2012, 23:1490-1497.
129. Lydiard R.B. Irritable bowel syndrome, anxiety, and depression: what are the links?. J Clin Psychiatry 2001, 62:38-45.
130. Levy R.L., Olden K.W., Naliboff B.D., Bradley L.A., Francisconi C., Drossman D.A., et al. Psychosocial aspects of functional gastrointestinal disorders. Gastroenterology 2006, 130:1447-1458.
131. Saito Y.A., Talley N.J. Genetics of irritable bowel syndrome. Am J Gastroenterol 2008, 103:2100-2104.
132. Chitkara D.K., van Tilburg M.A., Blois-Martin N., Whitehead W.E. Early life risk factors that contribute to irritable bowel syndrome in adults: a systematic review. Am J Gastroenterol 2008, 103:765-774.
133. Spiller R., Garsed K. Postinfectious irritable bowel syndrome. Gastroenterology 2009, 136:1979-1988.
134. Locke G.R., Zinsmeister A.R., Talley N.J., Fett S.L., Melton L.J. Familial association in adults with functional gastrointestinal disorders. Mayo Clin Proc 2000, 75:907-912.
135. Kalantar J.S., Locke G.R., Zinsmeister A.R., Beighley C.M., Talley N.J. Familial aggregation of irritable bowel syndrome: a prospective study. Gut 2003, 52:1703-1707.
136. Levy R.L., Whitehead W.E., von Korff M.R., Feld A.D. Intergenerational transmission of gastrointestinal illness behavior. Am J Gastroenterol 2000, 95:451-456.
137. Levy R.L., Jones K.R., Whitehead W.E., Feld S.I., Talley N.J., Corey L.A. Irritable bowel syndrome in twins: heredity and social learning both contribute to etiology. Gastroenterology 2001, 121:799-804.
138. Morris-Yates A., Talley N.J., Boyce P.M., Nandurkar S., Andrews G. Evidence of a genetic contribution to functional bowel disorders. Am J Gastroenterol 1998, 93:1311-1317.
139. Mohammed I., Cherkas L.F., Riley S.A., Spector T.D., Trudgill N.J. Genetic influences in irritable bowel syndrome: a twin study. Am J Gastroenterol 2005, 100:1340-1344.
140. Delvaux M., Denis P., Allemand H. Sexual abuse is more frequently reported by IBS patients than by patients with organic digestive diseases or controls. Results of a multicenter inquiry. French Club of Digestive Motility. Eur J Gastroenterol Hepatol 1997, 9:345-352.
141. Klooker T.K., Braak B., Painter R.C., de Rooij S.R., van Elburg R.M., van den Wijngaard R.M., et al. Exposure to severe wartime conditions in early life is associated with an increased risk of irritable bowel syndrome: a population-based cohort study. Am J Gastroenterol 2009, 104:2250-2256.
142. Ladd C.O., Huot R.L., Thrivikraman K.V., Nemeroff C.B., Meaney M.J., Plotsky P.M. Long-term behavioral and neuroendocrine adaptations to adverse early experience. Prog Brain Res 2000, 122:81-103.
143. Barreau F., Ferrier L., Fioramonti J., Bueno L. Neonatal maternal deprivation triggers long term alterations in colonic epithelial barrier and mucosal immunity in rats. Gut 2004, 53:501-506.
144. Coutinho S.V., Plotsky P.M., Sablad M., Miller J.C., Zhou H., Bayati A.I., et al. Neonatal maternal separation alters stress-induced responses to viscerosomatic nociceptive stimuli in rat. Am J Physiol Gastrointest Liver Physiol 2002, 282:G307-G316.
145. Videlock E.J., Adeyemo M., Licudine A., Hirano M., Ohning G., Mayer M., et al. Childhood trauma is associated with hypothalamic-pituitary-adrenal axis responsiveness in irritable bowel syndrome. Gastroenterology 2009, 137:1954-1962.
146. Piche T., Barbara G., Aubert P., Bruley des Varannes S., Dainese R., Nano J.L., et al. Impaired intestinal barrier integrity in the colon of patients with irritable bowel syndrome: involvement of soluble mediators. Gut 2009, 58:196-201.
147. Camilleri M., Lasch K., Zhou W. Irritable bowel syndrome: methods, mechanisms, and pathophysiology. The confluence of increased permeability, inflammation, and pain in irritable bowel syndrome. Am J Physiol Gastrointest Liver Physiol 2012, 303:G775-G785.
148. Barbara G., Stanghellini V., De Giorgio R., Cremon C., Cottrell G.S., Santini D., et al. Activated mast cells in proximity to colonic nerves correlate with abdominal pain in irritable bowel syndrome. Gastroenterology 2004, 126:693-702.
149. Francis D., Diorio J., Liu D., Meaney M.J. Nongenomic transmission across generations of maternal behavior and stress responses in the rat. Science 1999, 286:1155-1158.
150. Szyf M., McGowan P., Meaney M.J. The social environment and the epigenome. Environ Mol Mutagen 2008, 49:46-60.
151. Daniels W.M., Fairbairn L.R., van Tilburg G., McEvoy C.R., Zigmond M.J., Russell V.A., et al. Maternal separation alters nerve growth factor and corticosterone levels but not the DNA methylation status of the exon 1(7) glucocorticoid receptor promoter region. Metab Brain Dis 2009, 24:615-627.
152. McGowan P.O., Sasaki A., D'Alessio A.C., Dymov S., Labonté B., Szyf M., et al. Epigenetic regulation of the glucocorticoid receptor in human brain associates with childhood abuse. Nat Neurosci 2009, 12:342-348.
153. McGowan P.O., Sasaki A., Huang T.C., Unterberger A., Suderman M., Ernst C., et al. Promoter-wide hypermethylation of the ribosomal RNA gene promoter in the suicide brain. PLoS One 2008, 3:e2085.
154. van den Wijngaard R.M., Stanisor O.I., van Diest S.A., Welting O., Wouters M.M., Cailotto C., et al. Susceptibility to stress induced visceral hypersensitivity in maternally separated rats is transferred across generations. Neurogastroenterol Motil 2013, 25:e780-e790.
155. Murgatroyd C., Patchev A.V., Wu Y., Micale V., Bockmühl Y., Fischer D., et al. Dynamic DNA methylation programs persistent adverse effects of early life stress. Nat Neurosci 2009, 12:1559-1566.
156. Sandhu M.S., Luben R., Day N.E., Khaw K.T. Self-reported birth weight and subsequent risk of colorectal cancer. Cancer Epidemiol Biomarkers Prev 2002, 11:935-938.
157. Nilsen T.I., Romundstad P.R., Troisi R., Potischman N., Vatten L.J. Birth size and colorectal cancer risk: a prospective population based study. Gut 2005, 54:1728-1732.
158. Cnattingius S., Lundberg F., Iliadou A. Birth characteristics and risk of colorectal cancer: a study among Swedish twins. Br J Cancer 2009, 100:803-806.
159. Hughes L.A., van den Brandt P.A., de Bruïne A.P., Wouters K.A., Hulsmans S., Spiertz A., et al. Early life exposure to famine and colorectal cancer risk: a role for epigenetic mechanisms. PLoS One 2009, 4:e7951.
160. Sansom O.J., Stark L.A., Dunlop M.G., Clarke A.R. Suppression of intestinal and mammary neoplasia by lifetime administration of aspirin in Apc(Min/+) and Apc(Min/+), Msh2(?/?) mice. Cancer Res 2001, 61:7060-7064.
161. Charles M.A., Johnson I.T., Belshaw N.J. Supra-physiological folic acid concentrations induce aberrant DNA methylation in normal human cells in vitro. Epigenetics 2012, 7:689-694.
162. Bressenot A., Pooya S., Bossenmeyer-Pourie C., Gauchotte G., Germain A., Chevaux J.B., et al. Methyl donor deficiency affects small-intestinal differentiation and barrier function in rats. Br J Nutr 2013, 109:667-677.
163. Bauchart-Thevret C., Stoll B., Burrin D.G. Intestinal metabolism of sulfur amino acids. Nutr Res Rev 2009, 22:175-187.
164. +-coupled nutrient, micronutrient and drug transporters in the mammalian small intestine. Exp Physiol 2007, 92:603-619.
165. Trivedi M.S., Shah J.S., Al-Mughairy S., Hodgson N.W., Simms B., Trooskens G.A., et al. Food-derived opioid peptides inhibit cysteine uptake with redox and epigenetic consequences. J Nutr Biochem 2014, 25:1011-1018.
166. Waly M.I., Hornig M., Trivedi M., Hodgson N., Kini R., Ohta A., et al. Prenatal and postnatal epigenetic programming: implications for GI, immune, and neuronal function in autism. Autism Res Treat 2012, 2012:190930.
167. Teschemacher H. Opioid receptor ligands derived from food proteins. Curr Pharm Des 2003, 9:1331-1344.
168. Kaneko K., Iwasaki M., Yoshikawa M., Ohinata K. Orally administered soymorphins, soy-derived opioid peptides, suppress feeding and intestinal transit via gut mu(1)-receptor coupled to 5-HT(1A), D(2), and GABA(B) systems. Am J Physiol Gastrointest Liver Physiol 2010, 299:G799-G805.
169. Chung F.L., Conaway C.C., Rao C.V., Reddy B.S. Chemoprevention of colonic aberrant crypt foci in Fischer rats by sulforaphane and phenethyl isothiocyanate. Carcinogenesis 2000, 21:2287-2291.
170. Myzak M.C., Karplus P.A., Chung F.L., Dashwood R.H. A novel mechanism of chemoprotection by sulforaphane: inhibition of histone deacetylase. Cancer Res 2004, 64:5767-5774.
171. Rajendran P., Kidane A.I., Yu T.W., Dashwood W.M., Bisson W.H., Löhr C.V., et al. HDAC turnover, CtIP acetylation and dysregulated DNA damage signaling in colon cancer cells treated with sulforaphane and related dietary isothiocyanates. Epigenetics 2013, 8:612-623.
172. Myzak M.C., Dashwood W.M., Orner G.A., Ho E., Dashwood R.H. Sulforaphane inhibits histone deacetylase in vivo and suppresses tumorigenesis in Apc-minus mice. FASEB J 2006, 20:506-508.
173. Hu R., Khor T.O., Shen G., Jeong W.S., Hebbar V., Chen C., et al. Cancer chemoprevention of intestinal polyposis in ApcMin/+ mice by sulforaphane, a natural product derived from cruciferous vegetable. Carcinogenesis 2006, 27:2038-2046.
174. Myzak M.C., Tong P., Dashwood W.M., Dashwood R.H., Ho E. Sulforaphane retards the growth of human PC-3 xenografts and inhibits HDAC activity in human subjects. Exp Biol Med (Maywood) 2007, 232:227-234.
175. Druesne N., Pagniez A., Mayeur C., Thomas M., Cherbuy C., Duée P.H., et al. Diallyl disulfide (DADS) increases histone acetylation and p21(waf1/cip1) expression in human colon tumor cell lines. Carcinogenesis 2004, 25:1227-1236.
176. Druesne N., Pagniez A., Mayeur C., Thomas M., Cherbuy C., Duée P.H., et al. Repetitive treatments of colon HT-29 cells with diallyl disulfide induce a prolonged hyperacetylation of histone H3 K14. Ann NY Acad Sci 2004, 1030:612-621.
177. Druesne-Pecollo N., Chaumontet C., Pagniez A., Vaugelade P., Bruneau A., Thomas M., et al. in vivo treatment by diallyl disulfide increases histone acetylation in rat colonocytes. Biochem Biophys Res Commun 2007, 354:140-147.
178. Nian H., Delage B., Pinto J.T., Dashwood R.H. Allyl mercaptan, a garlic-derived organosulfur compound, inhibits histone deacetylase and enhances Sp3 binding on the P21WAF1 promoter. Carcinogenesis 2008, 29:1816-1824.
179. Lea M.A., Rasheed M., Randolph V.M., Khan F., Shareef A., desBordes C. Induction of histone acetylation and inhibition of growth of mouse erythroleukemia cells by S-allylmercaptocysteine. Nutr Cancer 2002, 43:90-102.
180. Li Y., Li X., Guo B. Chemopreventive agent 3,3?-diindolylmethane selectively induces proteasomal degradation of class I histone deacetylases. Cancer Res 2010, 70:646-654.
181. Joven J., Micol V., Segura-Carretero A., Alonso-Villaverde C., Menéndez J.A., Bioactive Food Components Platform Polyphenols and the modulation of gene expression pathways: can we eat our way out of the danger of chronic disease?. Crit Rev Food Sci Nutr 2014, 54:985-1001.
182. Fang M.Z., Wang Y., Ai N., Hou Z., Sun Y., Lu H., et al. Tea polyphenol (-)-epigallocatechin-3-gallate inhibits DNA methyltransferase and reactivates methylation-silenced genes in cancer cell lines. Cancer Res 2003, 63:7563-7570.
183. Waldecker M., Kautenburger T., Daumann H., Busch C., Schrenk D. Inhibition of histone-deacetylase activity by short-chain fatty acids and some polyphenol metabolites formed in the colon. J Nutr Biochem 2008, 19:587-593.
184. Wang L.S., Kuo C.T., Cho S.J., Seguin C., Siddiqui J., Stoner K., et al. Black raspberry-derived anthocyanins demethylate tumor suppressor genes through the inhibition of DNMT1 and DNMT3B in colon cancer cells. Nutr Cancer 2013, 65:118-125.
185. Wang L.S., Kuo C.T., Stoner K., Yearsley M., Oshima K., Yu J., et al. Dietary black raspberries modulate DNA methylation in dextran sodium sulfate (DSS)-induced ulcerative colitis. Carcinogenesis 2013, 34:2842-2850.
186. Wang L.S., Arnold M., Huang Y.W., Sardo C., Seguin C., Martin E., et al. Modulation of genetic and epigenetic biomarkers of colorectal cancer in humans by black raspberries: a phase I pilot study. Clin Cancer Res 2011, 17:598-610.
187. Tan S., Wang C., Lu C., Zhao B., Cui Y., Shi X., et al. Quercetin is able to demethylate the p16INK4a gene promoter. Chemotherapy 2009, 55:6-10.
188. Wang Z., Chen H. Genistein increases gene expression by demethylation of WNT5a promoter in colon cancer cell line SW1116. Anticancer Res 2010, 30:4537-4545.
189. Wang H., Li Q., Chen H. Genistein affects histone modifications on Dickkopf-related protein 1 (DKK1) gene in SW480 human colon cancer cell line. PLoS One 2012, 7:e40955.
190. Zhang Y., Li Q., Chen H. DNA methylation and histone modifications of Wnt genes by genistein during colon cancer development. Carcinogenesis 2013, 34:1756-1763.
191. Yara S., Lavoie J.C., Beaulieu J.F., Delvin E., Amre D., Marcil V., et al. Iron-ascorbate-mediated lipid peroxidation causes epigenetic changes in the antioxidant defense in intestinal epithelial cells: impact on inflammation. PLoS One 2013, 8:e63456.
192. Cyr A.R., Hitchler M.J., Domann F.E. Regulation of SOD2 in cancer by histone modifications and CpG methylation: closing the loop between redox biology and epigenetics. Antioxid Redox Signal 2013, 18:1946-1955.
193. Chen C., Wang L., Liao Q., Xu L., Huang Y., Zhang C., et al. Association between six genetic polymorphisms and colorectal cancer: a meta-analysis. Genet Test Mol Biomarkers 2014, 18:187-195.
194. Dashwood R.H. Frontiers in polyphenols and cancer prevention. J Nutr 2007, 137(1 Suppl.):267S-269S.
195. Min/+ mouse. Cancer Res 2007, 67:9937-9944.
196. Nair S., Hebbar V., Shen G., Gopalakrishnan A., Khor T.O., Yu S., et al. Synergistic effects of a combination of dietary factors sulforaphane and (-) epigallocatechin-3-gallate in HT-29 AP-1 human colon carcinoma cells. Pharm Res 2008, 25:387-399.