Postnatal epigenetic regulation of intestinal stem cells requires DNA methylation and is guided by the microbiome

Genome Biology

Volumn 16, Issue 1, 2015, Pages

  Yu, Da Hai ^a   Gadkari, Manasi ^a   Zhou, Quan ^a   Yu, Shiyan ^b   Gao, Nan ^b   Guan, Yongtao ^a   Schady, Deborah ^c   Roshan, Tony N ^a   Chen, Miao Hsueh ^a   Laritsky, Eleonora ^a   Ge, Zhongqi ^a   Wang, Hui ^a   Chen, Rui ^a   Westwater, Caroline ^d   Bry, Lynn ^e   Waterland, Robert A ^a   Moriarty, Chelsea ^a   Hwang, Cindy ^a   Swennes, Alton G ^a   Moore, Sean R ^f   Shen, Lanlan ^a   more..

^a BAYLOR COLLEGE OF MEDICINE   (United States)

^b RUTGERS UNIVERSITY   (United States)

^c TEXAS CHILDREN S HOSPITAL   (United States)

^d MEDICAL UNIVERSITY OF SOUTH CAROLINA   (United States)

^e BRIGHAM AND WOMEN S HOSPITAL   (United States)

^f CINCINNATI CHILDREN'S HOSPITAL MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DNA METHYLTRANSFERASE 1; DNA METHYLTRANSFERASE 3A; DNA (CYTOSINE 5) METHYLTRANSFERASE; DNA (CYTOSINE-5-)-METHYLTRANSFERASE 1;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL DIFFERENTIATION; CONTROLLED STUDY; CPG ISLAND; DNA METHYLATION; DNMT1 GENE; DNMT3A GENE; EPIGENETICS; FETUS; GENE SEQUENCE; GLYCOSYLATION; INTESTINAL STEM CELL; INTESTINE CRYPT; INTESTINE EPITHELIUM; MICROBIOME; MOUSE; NEWBORN; NONHUMAN; ORGANOGENESIS; POSTNATAL DEVELOPMENT; SUCKLING ANIMAL; TRANSCRIPTION INITIATION; TRANSCRIPTION REGULATION; ANIMAL; CYTOLOGY; GENETIC EPIGENESIS; GENETICS; INTESTINE; METABOLISM; MICROBIOLOGY; MICROFLORA; STEM CELL;

ANIMALS; ANIMALS, SUCKLING; CELL DIFFERENTIATION; CPG ISLANDS; DNA (CYTOSINE-5-)-METHYLTRANSFERASE; DNA METHYLATION; EPIGENESIS, GENETIC; INTESTINES; MICE; MICROBIOTA; STEM CELLS;

EID: 84942615814     PISSN: 14747596     EISSN: 1474760X     Source Type: Journal    
DOI: 10.1186/s13059-015-0763-5     Document Type: Article

References (67)

1. Cheng H, Bjerknes M. Whole population cell kinetics and postnatal development of the mouse intestinal epithelium. Anat Rec. 1985;211:420-6.
2. Cheng H, Leblond CP. Origin, differentiation and renewal of the four main epithelial cell types in the mouse small intestine. V. Unitarian Theory of the origin of the four epithelial cell types. Am J Anat. 1974;141:537-61.
3. Henning SJ. Postnatal development: coordination of feeding, digestion, and metabolism. Am J Physiol. 1981;241:G199-214.
4. Barker N, van Es JH, Kuipers J, Kujala P, van den Born M, Cozijnsen M, et al. Identification of stem cells in small intestine and colon by marker gene Lgr5. Nature. 2007;449:1003-7.
5. Sheaffer KL, Kaestner KH. Transcriptional networks in liver and intestinal development. Cold Spring Harb Perspect Biol. 2012;4:a008284.
6. Gu B, Watanabe K, Dai X. Epithelial stem cells: an epigenetic and Wnt-centric perspective. J Cell Biochem. 2010;110:1279-87.
7. Kaaij LT, van de Wetering M, Fang F, Decato B, Molaro A, van de Werken HJ, et al. DNA methylation dynamics during intestinal stem cell differentiation reveals enhancers driving gene expression in the villus. Genome Biol. 2013;14:R50.
8. Kim TH, Li F, Ferreiro-Neira I, Ho LL, Luyten A, Nalapareddy K, et al. Broadly permissive intestinal chromatin underlies lateral inhibition and cell plasticity. Nature. 2014;506:511-5.
9. Sheaffer KL, Kim R, Aoki R, Elliott EN, Schug J, Burger L, et al. DNA methylation is required for the control of stem cell differentiation in the small intestine. Genes Dev. 2014;28:652-64.
10. Waterland RA. Epigenetic mechanisms and gastrointestinal development. J Pediatr. 2006;149:S137-142.
11. Jones PA. Functions of DNA methylation: islands, start sites, gene bodies and beyond. Nat Rev Genet. 2012;13:484-92.
12. Deaton AM, Bird A. CpG islands and the regulation of transcription. Genes Dev. 2011;25:1010-22.
13. Yu DH, Ware C, Waterland RA, Zhang J, Chen MH, Gadkari M, et al. Developmentally programmed 3' CpG island methylation confers tissue- and cell-type-specific transcriptional activation. Mol Cell Biol. 2013;33:1845-58.
14. Waterland RA, Michels KB. Epigenetic epidemiology of the developmental origins hypothesis. Annu Rev Nutr. 2007;27:363-88.
15. Chang L, Neu J. Early factors leading to later obesity: interactions of the microbiome, epigenome, and nutrition. Curr Probl Pediatr Adolesc Health Care. 2015;45:134-42.
16. Mudd SH, Brosnan JT, Brosnan ME, Jacobs RL, Stabler SP, Allen RH, et al. Methyl balance and transmethylation fluxes in humans. Am J Clin Nutr. 2007;85:19-25.
17. Stover PJ. Polymorphisms in 1-carbon metabolism, epigenetics and folate-related pathologies. J Nutrigenet Nutrigenomics. 2011;4:293-305.
18. Abrams GD, Bauer H, Sprinz H. Influence of the normal flora on mucosal morphology and cellular renewal in the ileum. A comparison of germ-free and conventional mice. Lab Invest. 1963;12:355-64.
19. Stappenbeck TS, Hooper LV, Gordon JI. Developmental regulation of intestinal angiogenesis by indigenous microbes via Paneth cells. Proc Natl Acad Sci U S A. 2002;99:15451-5.
20. Bry L, Falk PG, Midtvedt T, Gordon JI. A model of host-microbial interactions in an open mammalian ecosystem. Science. 1996;273:1380-3.
21. Freitas M, Axelsson LG, Cayuela C, Midtvedt T, Trugnan G. Microbial-host interactions specifically control the glycosylation pattern in intestinal mouse mucosa. Histochem Cell Biol. 2002;118:149-61.
22. Rakoff-Nahoum S, Kong Y, Kleinstein SH, Subramanian S, Ahern PP, Gordon JI, et al. Analysis of gene-environment interactions in postnatal development of the mammalian intestine. Proc Natl Acad Sci U S A. 2015;112:1929-36.
23. Sommer F, Backhed F. The gut microbiota--masters of host development and physiology. Nat Rev Microbiol. 2013;11:227-38.
24. Banasaz M, Norin E, Holma R, Midtvedt T. Increased enterocyte production in gnotobiotic rats mono-associated with Lactobacillus rhamnosus GG. Appl Environ Microbiol. 2002;68:3031-4.
25. Buchon N, Broderick NA, Chakrabarti S, Lemaitre B. Invasive and indigenous microbiota impact intestinal stem cell activity through multiple pathways in Drosophila. Genes Dev. 2009;23:2333-44.
26. Savage DC, Siegel JE, Snellen JE, Whitt DD. Transit time of epithelial cells in the small intestines of germfree mice and ex-germfree mice associated with indigenous microorganisms. Appl Environ Microbiol. 1981;42:996-1001.
27. Kau AL, Ahern PP, Griffin NW, Goodman AL, Gordon JI. Human nutrition, the gut microbiome and the immune system. Nature. 2011;474:327-36.
28. 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:R1065-1069.
29. Takahashi K. Influence of bacteria on epigenetic gene control. Cell Mol Life Sci. 2014;71:1045-54.
30. 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;286:35755-62.
31. Kumar H, Lund R, Laiho A, Lundelin K, Ley RE, Isolauri E, et al. Gut microbiota as an epigenetic regulator: pilot study based on whole-genome methylation analysis. MBio. 2014;5(6):e02113-14. PMID: 25516615, PMCID: PMC4271550.
32. Itzkovitz S, Blat IC, Jacks T, Clevers H, van Oudenaarden A. Optimality in the development of intestinal crypts. Cell. 2012;148:608-19.
33. Kunde-Ramamoorthy G, Coarfa C, Laritsky E, Kessler NJ, Harris RA, Xu M, et al. Comparison and quantitative verification of mapping algorithms for whole-genome bisulfite sequencing. Nucleic Acids Res. 2014;42:e43.
34. Jenke AC, Postberg J, Raine T, Nayak KM, Molitor M, Wirth S, et al. DNA methylation analysis in the intestinal epithelium-effect of cell separation on gene expression and methylation profile. PLoS One. 2013;8:e55636.
35. Kemper K, Prasetyanti PR, De Lau W, Rodermond H, Clevers H, Medema JP. Monoclonal antibodies against Lgr5 identify human colorectal cancer stem cells. Stem Cells. 2012;30:2378-86.
36. Magness ST, Puthoff BJ, Crissey MA, Dunn J, Henning SJ, Houchen C, et al. A multicenter study to standardize reporting and analyses of fluorescence-activated cell-sorted murine intestinal epithelial cells. Am J Physiol Gastrointest Liver Physiol. 2013;305:G542-551.
37. Biol-N'garagba MC, Louisot P. Regulation of the intestinal glycoprotein glycosylation during postnatal development: role of hormonal and nutritional factors. Biochimie. 2003;85:331-52.
38. Haltiwanger RS, Lowe JB. Role of glycosylation in development. Annu Rev Biochem. 2004;73:491-537.
39. Doi A, Park IH, Wen B, Murakami P, Aryee MJ, Irizarry R, et al. Differential methylation of tissue- and cancer-specific CpG island shores distinguishes human induced pluripotent stem cells, embryonic stem cells and fibroblasts. Nat Genet. 2009;41:1350-3.
40. Koo BK, Spit M, Jordens I, Low TY, Stange DE, van de Wetering M, et al. Tumour suppressor RNF43 is a stem-cell E3 ligase that induces endocytosis of Wnt receptors. Nature. 2012;488:665-9.
41. Lin S, Yeruva S, He P, Singh AK, Zhang H, Chen M, et al. Lysophosphatidic acid stimulates the intestinal brush border Na(+)/H(+) exchanger 3 and fluid absorption via LPA(5) and NHERF2. Gastroenterology. 2010;138:649-58.
42. Chen T, Li E. Structure and function of eukaryotic DNA methyltransferases. Curr Top Dev Biol. 2004;60:55-89.
43. Kellermayer R, Balasa A, Zhang W, Lee S, Mirza S, Chakravarty A, et al. Epigenetic maturation in colonic mucosa continues beyond infancy in mice. Hum Mol Genet. 2010;19:2168.
44. Li G, Zhang W, Baker MS, Laritsky E, Mattan-Hung N, Yu D, et al. Major epigenetic development distinguishing neuronal and non-neuronal cells occurs postnatally in the murine hypothalamus. Hum Mol Genet. 2014;23:1579-90.
45. Fatemi M, Hermann A, Gowher H, Jeltsch A. Dnmt3a and Dnmt1 functionally cooperate during de novo methylation of DNA. Eur J Biochem. 2002;269:4981-4.
46. Jair KW, Bachman KE, Suzuki H, Ting AH, Rhee I, Yen RW, et al. De novo CpG island methylation in human cancer cells. Cancer Res. 2006;66:682-92.
47. Campbell BJ, Yu LG, Rhodes JM. Altered glycosylation in inflammatory bowel disease: a possible role in cancer development. Glycoconj J. 2001;18:851-8.
48. Dai D, Nanthkumar NN, Newburg DS, Walker WA. Role of oligosaccharides and glycoconjugates in intestinal host defense. J Pediatr Gastroenterol Nutr. 2000;30:S23-33.
49. Dall'Olio F, Malagolini N, Di Stefano G, Ciambella M, Serafini-Cessi F. Postnatal development of rat colon epithelial cells is associated with changes in the expression of the beta 1,4-N-acetylgalactosaminyltransferase involved in the synthesis of Sda antigen of alpha 2,6-sialyltransferase activity towards N-acetyl-lactosamine. Biochem J. 1990;270:519-24.
50. Kawamura YI, Kawashima R, Fukunaga R, Hirai K, Toyama-Sorimachi N, Tokuhara M, et al. Introduction of Sd(a) carbohydrate antigen in gastrointestinal cancer cells eliminates selectin ligands and inhibits metastasis. Cancer Res. 2005;65:6220-7.
51. Kim YS, Isaacs R. Glycoprotein metabolism in inflammatory and neoplastic diseases of the human colon. Cancer Res. 1975;35:2092-7.
52. Gordon HA, Pesti L. The gnotobiotic animal as a tool in the study of host microbial relationships. Bacteriol Rev. 1971;35:390-429.
53. Hooper LV, Gordon JI. Glycans as legislators of host-microbial interactions: spanning the spectrum from symbiosis to pathogenicity. Glycobiology. 2001;11:1R-10R.
54. Madison BB, Dunbar L, Qiao XT, Braunstein K, Braunstein E, Gumucio DL. Cis elements of the villin gene control expression in restricted domains of the vertical (crypt) and horizontal (duodenum, cecum) axes of the intestine. J Biol Chem. 2002;277:33275-83.
55. Challen GA, Sun D, Jeong M, Luo M, Jelinek J, Berg JS, et al. Dnmt3a is essential for hematopoietic stem cell differentiation. Nat Genet. 2012;44:23-31.
56. Feng J, Zhou Y, Campbell SL, Le T, Li E, Sweatt JD, et al. Dnmt1 and Dnmt3a maintain DNA methylation and regulate synaptic function in adult forebrain neurons. Nat Neurosci. 2010;13:423-30.
57. Kaneda M, Okano M, Hata K, Sado T, Tsujimoto N, Li E, et al. Essential role for de novo DNA methyltransferase Dnmt3a in paternal and maternal imprinting. Nature. 2004;429:900-3.
58. Jackson-Grusby L, Beard C, Possemato R, Tudor M, Fambrough D, Csankovszki G, et al. Loss of genomic methylation causes p53-dependent apoptosis and epigenetic deregulation. Nat Genet. 2001;27:31-9.
59. Krueger F, Andrews SR. Bismark: a flexible aligner and methylation caller for Bisulfite-Seq applications. Bioinformatics. 2011;27:1571-2.
60. Seisenberger S, Andrews S, Krueger F, Arand J, Walter J, Santos F, et al. The dynamics of genome-wide DNA methylation reprogramming in mouse primordial germ cells. Mol Cell. 2012;48:849-62.
61. Langmead B, Salzberg SL. Fast gapped-read alignment with Bowtie 2. Nat Methods. 2012;9:357-9.
62. Trapnell C, Williams BA, Pertea G, Mortazavi A, Kwan G, van Baren MJ, et al. Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat Biotechnol. 2010;28:511-5.
63. Colella S, Shen L, Baggerly KA, Issa JP, Krahe R. Sensitive and quantitative universal Pyrosequencing methylation analysis of CpG sites. Biotechniques. 2003;35:146-50.
64. Shen L, Guo Y, Chen X, Ahmed S, Issa JP. Optimizing annealing temperature overcomes bias in bisulfite PCR methylation analysis. Biotechniques. 2007;42:48, 50, 52 passim.
65. Sakamori R, Das S, Yu S, Feng S, Stypulkowski E, Guan Y, et al. Cdc42 and Rab8a are critical for intestinal stem cell division, survival, and differentiation in mice. J Clin Invest. 2012;122:1052-65.
66. Illingworth RS, Gruenewald-Schneider U, Webb S, Kerr AR, James KD, Turner DJ, et al. Orphan CpG islands identify numerous conserved promoters in the mammalian genome. PLoS Genet. 2010;6:e1001134.
67. DAVID. https://david.ncifcrf.gov/.