Marked methylation changes in intestinal genes during the perinatal period of preterm neonates

BMC Genomics

Volumn 15, Issue 1, 2014, Pages

  Gao, Fei ^a   Zhang, Juyong ^a   Jiang, Pingping ^b   Gong, Desheng ^a   Wang, Jun Wen ^a   Xia, Yudong ^a   Østergaard, Mette V ^b   Wang, Jun ^a,b,c,d   Sangild, Per T ^b  

^a BGI SHENZHEN   (China)

^b UNIVERSITY OF COPENHAGEN   (Denmark)

^c KING ABDULAZIZ UNIVERSITY   (Saudi Arabia)

^d Capital Region   (Denmark)

Author keywords

DNA methylation; Necrotizing enterocolitis; Preterm neonates

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ARTIFICIAL MILK; CEND1 GENE; CYP2W1 GENE; DNA METHYLATION; DNA SEQUENCE; DOWN REGULATION; GENE; GENE EXPRESSION; GENETIC TRANSCRIPTION; GPR146 GENE; INTESTINE; METABOLISM; NECROTIZING ENTEROCOLITIS; NEWBORN; NONHUMAN; NUCLEOTIDE SEQUENCE; PERINATAL PERIOD; POLYMERASE CHAIN REACTION; PREMATURITY; PRENATAL PERIOD; PROMOTER REGION; TOP1MT GENE; ANIMAL; FEMALE; GENETIC EPIGENESIS; GENETICS; GESTATIONAL AGE; HUMAN; PIG;

ANIMALS; ANIMALS, NEWBORN; DNA METHYLATION; ENTEROCOLITIS, NECROTIZING; EPIGENESIS, GENETIC; FEMALE; GESTATIONAL AGE; HUMANS; INTESTINES; PREMATURE BIRTH; PROMOTER REGIONS, GENETIC; SEQUENCE ANALYSIS, DNA; SUS SCROFA;

EID: 84906931614     PISSN: None     EISSN: 14712164     Source Type: Journal    
DOI: 10.1186/1471-2164-15-716     Document Type: Article

References (56)

1. Goldberg AD, Allis CD, Bernstein E. Epigenetics: a landscape takes shape. Cell 2007, 128(4):635-638.
2. Suzuki MM, Bird A. DNA methylation landscapes: provocative insights from epigenomics. Nat Rev Genet 2008, 9(6):465-476.
3. Morgan HD, Santos F, Green K, Dean W, Reik W. Epigenetic reprogramming in mammals. Hum Mol Genet 2005, 14(Spec No 1):R47-R58.
4. Anderson OS, Sant KE, Dolinoy DC. Nutrition and epigenetics: an interplay of dietary methyl donors, one-carbon metabolism and DNA methylation. J Nutr Biochem 2012, 23(8):853-859.
5. Sangild PT. Gut responses to enteral nutrition in preterm infants and animals. Exp Biol Med (Maywood) 2006, 231(11):1695-1711.
6. Henry MC, Moss RL. Neonatal necrotizing enterocolitis. Semin Pediatr Surg 2008, 17(2):98-109.
7. Bjornvad CR, Schmidt M, Petersen YM, Jensen SK, Offenberg H, Elnif J, Sangild PT. Preterm birth makes the immature intestine sensitive to feeding-induced intestinal atrophy. Am J Physiol Regul Integr Comp Physiol 2005, 289(4):R1212-R1222.
8. Jiang P, Wan JM, Cilieborg MS, Sit WH, Sangild PT. Premature delivery reduces intestinal cytoskeleton, metabolism, and stress response proteins in newborn formula-fed pigs. J Pediatr Gastroenterol Nutr 2013, 56(6):615-622.
9. Siggers J, Sangild PT, Jensen TK, Siggers RH, Skovgaard K, Stoy AC, Jensen BB, Thymann T, Bering SB, Boye M. Transition from parenteral to enteral nutrition induces immediate diet-dependent gut histological and immunological responses in preterm neonates. Am J Physiol Gastrointest Liver Physiol 2011, 301(3):G435-G445.
10. Jiang P, Siggers JL, Ngai HH, Sit WH, Sangild PT, Wan JM. The small intestine proteome is changed in preterm pigs developing necrotizing enterocolitis in response to formula feeding. J Nutr 2008, 138(10):1895-1901.
11. Blencowe H, Cousens S, Oestergaard MZ, Chou D, Moller AB, Narwal R, Adler A, Vera Garcia C, Rohde S, Say L, Lawn JE. National, regional, and worldwide estimates of preterm birth rates in the year 2010 with time trends since 1990 for selected countries: a systematic analysis and implications. Lancet 2012, 379(9832):2162-2172.
12. Morgan J, Young L, McGuire W. Delayed introduction of progressive enteral feeds to prevent necrotising enterocolitis in very low birth weight infants. Cochrane Database Syst Rev 2013, 5. CD001970.
13. Jiang P, Sangild PT, Siggers RH, Sit WH, Lee CL, Wan JM. Bacterial colonization affects the intestinal proteome of preterm pigs susceptible to necrotizing enterocolitis. Neonatology 2011, 99(4):280-288.
14. Bjornvad CR, Thymann T, Deutz NE, Burrin DG, Jensen SK, Jensen BB, Molbak L, Boye M, Larsson LI, Schmidt M, Michaelsen KF, Sangild PT. Enteral feeding induces diet-dependent mucosal dysfunction, bacterial proliferation, and necrotizing enterocolitis in preterm pigs on parenteral nutrition. Am J Physiol Gastrointest Liver Physiol 2008, 295(5):G1092-G1103.
15. Sangild PT, Petersen YM, Schmidt M, Elnif J, Petersen TK, Buddington RK, Greisen G, Michaelsen KF, Burrin DG. Preterm birth affects the intestinal response to parenteral and enteral nutrition in newborn pigs. J Nutr 2002, 132(12):3786-3794.
16. Li Y, Ostergaard MV, Jiang P, Chatterton DE, Thymann T, Kvistgaard AS, Sangild PT. Whey Protein Processing Influences Formula-Induced Gut Maturation in Preterm Pigs. J Nutr 2013, 143(12):1934-1942.
17. Meissner A, Mikkelsen TS, Gu H, Wernig M, Hanna J, Sivachenko A, Zhang X, Bernstein BE, Nusbaum C, Jaffe DB, Gnirke A, Jaenisch R, Lander ES. Genome-scale DNA methylation maps of pluripotent and differentiated cells. Nature 2008, 454(7205):766-770.
18. Meissner A, Gnirke A, Bell GW, Ramsahoye B, Lander ES, Jaenisch R. Reduced representation bisulfite sequencing for comparative high-resolution DNA methylation analysis. Nucleic Acids Res 2005, 33(18):5868-5877.
19. Wang L, Sun J, Wu H, Liu S, Wang J, Wu B, Huang S, Li N, Zhang X. Systematic assessment of reduced representation bisulfite sequencing to human blood samples: A promising method for large-sample-scale epigenomic studies. J Biotechnol 2012, 157(1):1-6.
20. Wang J, Xia Y, Li L, Gong D, Yao Y, Luo H, Lu H, Yi N, Wu H, Zhang X, Tao Q, Gao F. Double restriction-enzyme digestion improves the coverage and accuracy of genome-wide CpG methylation profiling by reduced representation bisulfite sequencing. BMC Genomics 2013, 14:11.
21. Bird A. DNA methylation patterns and epigenetic memory. Genes Dev 2002, 16(1):6-21.
22. Suzuki R, Shimodaira H. Pvclust: an R package for assessing the uncertainty in hierarchical clustering. Bioinformatics 2006, 22(12):1540-1542.
23. Li Y, Zhu J, Tian G, Li N, Li Q, Ye M, Zheng H, Yu J, Wu H, Sun J, Zhang H, Chen Q, Luo R, Chen M, He Y, Jin X, Zhang Q, Yu C, Zhou G, Sun J, Huang Y, Zheng H, Cao H, Zhou X, Guo S, Hu X, Li X, Kristiansen K, Bolund L, Xu J. The DNA methylome of human peripheral blood mononuclear cells. PLoS Biol 2010, 8(11):e1000533.
24. Chow JC, Yen Z, Ziesche SM, Brown CJ. Silencing of the mammalian X chromosome. Annu Rev Genomics Hum Genet 2005, 6:69-92.
25. Zhang B, Kirov S, Snoddy J. WebGestalt: an integrated system for exploring gene sets in various biological contexts. Nucleic Acids Res 2005, 33(Web Server issue):W741-W748.
26. Wang J, Duncan D, Shi Z, Zhang B. WEB-based GEne SeT AnaLysis Toolkit (WebGestalt): update 2013. Nucleic Acids Res 2013, 41(Web Server issue):W77-W83.
27. Waterland RA. Epigenetic mechanisms and gastrointestinal development. J Pediatr 2006, 149(5 Suppl):S137-S142.
28. Reed K, Poulin ML, Yan L, Parissenti AM. Comparison of bisulfite sequencing PCR with pyrosequencing for measuring differences in DNA methylation. Anal Biochem 2010, 397(1):96-106.
29. Hafner M, Rezen T, Rozman D. Regulation of hepatic cytochromes p450 by lipids and cholesterol. Curr Drug Metab 2011, 12(2):173-185.
30. Reimann F, Tolhurst G, Gribble FM. G-protein-coupled receptors in intestinal chemosensation. Cell Metab 2012, 15(4):421-431.
31. Douarre C, Sourbier C, Dalla Rosa I, Brata Das B, Redon CE, Zhang H, Neckers L, Pommier Y. Mitochondrial topoisomerase I is critical for mitochondrial integrity and cellular energy metabolism. PLoS One 2012, 7(7):e41094.
32. Makri G, Lavdas AA, Katsimpardi L, Charneau P, Thomaidou D, Matsas R. Transplantation of embryonic neural stem/precursor cells overexpressing BM88/Cend1 enhances the generation of neuronal cells in the injured mouse cortex. Stem Cells 2010, 28(1):127-139.
33. De Santa BP, van den Brink GR, Roberts DJ. Development and differentiation of the intestinal epithelium. Cell Mol Life Sci 2003, 60(7):1322-1332.
34. Martino D, Loke YJ, Gordon L, Ollikainen M, Cruickshank MN, Saffery R, Craig JM. Longitudinal, genome-scale analysis of DNA methylation in twins from birth to 18 months of age reveals rapid epigenetic change in early life and pair-specific effects of discordance. Genome Biol 2013, 14(5):R42.
35. Heyn H, Li N, Ferreira HJ, Moran S, Pisano DG, Gomez A, Diez J, Sanchez-Mut JV, Setien F, Carmona FJ, Puca AA, Sayols S, Pujana MA, Serra-Musach J, Iglesias-Platas I, Formiga F, Fernandez AF, Fraga MF, Heath SC, Valencia A, Gut IG, Wang J, Esteller M. Distinct DNA methylomes of newborns and centenarians. Proc Natl Acad Sci U S A 2012, 109(26):10522-10527.
36. Sangild PT, Thymann T, Schmidt M, Stoll B, Burrin DG, Buddington RK. Invited review: the preterm pig as a model in pediatric gastroenterology. J Anim Sci 2013, 91(10):4713-4729.
37. Tsui DW, Chiu RW, Lo YD. Epigenetic approaches for the detection of fetal DNA in maternal plasma. Chimerism 2010, 1(1):30-35.
38. Sangild PT, Siggers RH, Schmidt M, Elnif J, Bjornvad CR, Thymann T, Grondahl ML, Hansen AK, Jensen SK, Boye M, Moelbak L, Buddington RK, Westro¨m BR, Holst JJ, Burrin DG. Diet- and colonization-dependent intestinal dysfunction predisposes to necrotizing enterocolitis in preterm pigs. Gastroenterology 2006, 130(6):1776-1792.
39. Sato N. Central role of mitochondria in metabolic regulation of liver pathophysiology. J Gastroenterol Hepatol 2007, 22(Suppl 1):S1-S6.
40. Pacha J. Development of intestinal transport function in mammals. Physiol Rev 2000, 80(4):1633-1667.
41. Ade-Ajayi N, Spitz L, Kiely E, Drake D, Klein N. Intestinal glycosaminoglycans in neonatal necrotizing enterocolitis. Br J Surg 1996, 83(3):415-418.
42. Koropatkin NM, Cameron EA, Martens EC. How glycan metabolism shapes the human gut microbiota. Nat Rev Microbiol 2012, 10(5):323-335.
43. Puiman PJ, Jensen M, Stoll B, Renes IB, De Bruijn AC, Dorst K, Schierbeek H, Schmidt M, Boehm G, Burrin DG, Sangild PT, van Goudoever JB. Intestinal threonine utilization for protein and mucin synthesis is decreased in formula-fed preterm pigs. J Nutr 2011, 141(7):1306-1311.
44. Janeway CA, Medzhitov R. Innate immune recognition. Annu Rev Immunol 2002, 20:197-216.
45. Menon R, Conneely KN, Smith AK. DNA methylation: an epigenetic risk factor in preterm birth. Reprod Sci 2012, 19(1):6-13.
46. Mizutani Y, Kihara A, Igarashi Y. Identification of the human sphingolipid C4-hydroxylase, hDES2, and its up-regulation during keratinocyte differentiation. FEBS Lett 2004, 563(1-3):93-97.
47. Moller HK, Thymann T, Fink LN, Frokiaer H, Kvistgaard AS, Sangild PT. Bovine colostrum is superior to enriched formulas in stimulating intestinal function and necrotising enterocolitis resistance in preterm pigs. Br J Nutr 2011, 105(1):44-53.
48. Mace OJ, Marshall F. Digestive physiology of the pig symposium: gut chemosensing and the regulation of nutrient absorption and energy supply. J Anim Sci 2013, 91(5):1932-1945.
49. Yosten GL, Kolar GR, Redlinger LJ, Samson WK. Evidence for an interaction between proinsulin C-peptide and GPR146. J Endocrinol 2013, 218(2):B1-B8.
50. Bertino E, Arslanoglu S, Martano C, Di Nicola P, Giuliani F, Peila C, Cester E, Pirra A, Coscia A, Moro G. Biological, nutritional and clinical aspects of feeding preterm infants with human milk. J Biol Regul Homeost Agents 2012, 26(3 Suppl):9-13.
51. Zhou J, Li J, Chen J, Liu Y, Gao W, Ding Y. Over-expression of CDH22 is associated with tumor progression in colorectal cancer. Tumour Biol 2009, 30(3):130-140.
52. Jostins L, Ripke S, Weersma RK, Duerr RH, McGovern DP, Hui KY, Lee JC, Schumm LP, Sharma Y, Anderson CA, Essers J, Mitrovic M, Ning K, Cleynen I, Theatre E, Spain SL, Raychaudhuri S, Goyette P, Wei Z, Abraham C, Achkar JP, Ahmad T, Amininejad L, Ananthakrishnan AN, Andersen V, Andrews JM, Baidoo L, Balschun T, Bampton PA, Bitton A. Host-microbe interactions have shaped the genetic architecture of inflammatory bowel disease. Nature 2012, 491(7422):119-124.
53. Li R, Yu C, Li Y, Lam TW, Yiu SM, Kristiansen K, Wang J. SOAP2: an improved ultrafast tool for short read alignment. Bioinformatics 2009, 25(15):1966-1967.
54. Lister R, Pelizzola M, Dowen RH, Hawkins RD, Hon G, Tonti-Filippini J, Nery JR, Lee L, Ye Z, Ngo QM, Edsall L, Antosiewicz-Bourget J, Stewart R, Ruotti V, Millar AH, Thomson JA, Ren B, Ecker JR. Human DNA methylomes at base resolution show widespread epigenomic differences. Nature 2009, 462(7271):315-322.
55. Benjamini Y, Hochberg Y. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J Royal Stat Soc 1995, 57:289-300.
56. Gao F, Zhang J, Gong D. Data showing marked methylation changes of intestinal genes in the neonatal period of preterm neonates. Giga Sci Database 2013,