Cryosectioning the intestinal crypt-villus axis: An ex vivo method to study the dynamics of epigenetic modifications from stem cells to differentiated cells

Stem Cell Research

Volumn 14, Issue 1, 2015, Pages 105-113

  Vincent, Audrey ^a,b,c   Kazmierczak, Catherine ^a,b,c   Duchêne, Belinda ^a,b,c   Jonckheere, Nicolas ^a,b,c   Leteurtre, Emmanuelle ^a,b,c   Van Seuningen, Isabelle ^a,b,c  

^a JEAN PIERRE AUBERT RESEARCH CENTER   (France)

^b UNIV LILLE   (France)

^c LILLE UNIVERSITY HOSPITAL   (France)

Author keywords

[No Author keywords available]

Indexed keywords

DNA; MUCIN 2; TRANSCRIPTION FACTOR CDX2; TRANSCRIPTION FACTOR SOX9; ASCL2 PROTEIN, MOUSE; BASIC HELIX LOOP HELIX TRANSCRIPTION FACTOR; BMI1 PROTEIN; BMI1 PROTEIN, MOUSE; CDX2 PROTEIN, MOUSE; G PROTEIN COUPLED RECEPTOR; HISTONE; HOMEODOMAIN PROTEIN; LGR5 PROTEIN, MOUSE; MUC2 PROTEIN, MOUSE; ONCOPROTEIN; TRANSCRIPTION FACTOR;

ANIMAL EXPERIMENT; ARTICLE; CELL DIFFERENTIATION; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; CRYOSECTIONING; DNA METHYLATION; EPIGENETICS; EX VIVO STUDY; FROZEN SECTION; GENE EXPRESSION; HISTONE MODIFICATION; INTESTINAL STEM CELL; INTESTINE CELL; INTESTINE CRYPT; INTESTINE VILLUS; MOUSE; NONHUMAN; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; ANIMAL; C57BL MOUSE; CHORION VILLUS; CPG ISLAND; CYTOLOGY; GENETIC EPIGENESIS; GENETICS; INTESTINE MUCOSA; METABOLISM; PATHOLOGY; PROMOTER REGION; STEM CELL;

ANIMALS; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; CELL DIFFERENTIATION; CHORIONIC VILLI; CPG ISLANDS; DNA METHYLATION; EPIGENESIS, GENETIC; GENE EXPRESSION; HISTONES; HOMEODOMAIN PROTEINS; INTESTINAL MUCOSA; MICE; MICE, INBRED C57BL; MUCIN-2; POLYCOMB REPRESSIVE COMPLEX 1; PROMOTER REGIONS, GENETIC; PROTO-ONCOGENE PROTEINS; RECEPTORS, G-PROTEIN-COUPLED; SOX9 TRANSCRIPTION FACTOR; STEM CELLS; TRANSCRIPTION FACTORS;

EID: 84922647532     PISSN: 18735061     EISSN: 18767753     Source Type: Journal    
DOI: 10.1016/j.scr.2014.12.002     Document Type: Article

References (43)

1. Allegrucci C., Wu Y.Z., Thurston A., et al. Restriction landmark genome scanning identifies culture-induced DNA methylation instability in the human embryonic stem cell epigenome. Hum Mol Genet 2007, 16(10):1253-1268. (ddm074 [pii]). 10.1093/hmg/ddm074.
2. Barker N., van Es J.H., Kuipers J., et al. Identification of stem cells in small intestine and colon by marker gene Lgr5. Nature 2007, 449(7165):1003-1007. (nature06196 [pii]). 10.1038/nature06196.
3. Barnard J.A., Beauchamp R.D., Coffey R.J., Moses H.L. Regulation of intestinal epithelial cell growth by transforming growth factor type beta. Proc Natl Acad Sci U S A 1989, 86(5):1578-1582. (Available at: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=286741&tool=pmcentrez&rendertype=abstract. Accessed September 2, 2014).
4. Benoit Y.D., Paré F., Francoeur C., et al. Cooperation between HNF-1alpha, Cdx2, and GATA-4 in initiating an enterocytic differentiation program in a normal human intestinal epithelial progenitor cell line. Am J Physiol Gastrointest Liver Physiol 2010, 298(4):G504-G517. 10.1152/ajpgi.00265.2009.
5. Benoit Y.D., Lepage M.B., Khalfaoui T., et al. Polycomb repressive complex 2 impedes intestinal cell terminal differentiation. J Cell Sci 2012, 125(Pt 14):3454-3463. 10.1242/jcs.102061.
6. Berdasco M., Esteller M. DNA methylation in stem cell renewal and multipotency. Stem Cell Res Ther 2011, 2(5):42. 10.1186/scrt83.
7. Bernstein B.E., Mikkelsen T.S., Xie X., et al. A bivalent chromatin structure marks key developmental genes in embryonic stem cells. Cell 2006, 125(2):315-326. (S0092-8674(06)00380-1 [pii]). 10.1016/j.cell.2006.02.041.
8. Bibikova M., Chudin E., Wu B., et al. Human embryonic stem cells have a unique epigenetic signature. Genome Res 2006, 16(9):1075-1083. (gr.5319906 [pii]). 10.1101/gr.5319906.
9. Blache P., van de Wetering M., Duluc I., et al. SOX9 is an intestine crypt transcription factor, is regulated by the Wnt pathway, and represses the CDX2 and MUC2 genes. J Cell Biol 2004, 166(1):37-47. (Available at: http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=PubMed&dopt=Citation&list_uids=15240568).
10. Buisine M.P., Devisme L., Maunoury V., et al. Developmental mucin gene expression in the gastroduodenal tract and accessory digestive glands. I. Stomach. A relationship to gastric carcinoma. J Histochem Cytochem 2000, 48(12):1657-1666. (Available at: http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=PubMed&dopt=Citation&list_uids=11101634).
11. Chawengsaksophak K., James R., Hammond V.E., Kontgen F., Beck F. Homeosis and intestinal tumours in Cdx2 mutant mice. Nature 1997, 386(6620):84-87. (Available at: http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=PubMed&dopt=Citation&list_uids=9052785).
12. Clevers H. The intestinal crypt, a prototype stem cell compartment. Cell 2013, 154(2):274-284. 10.1016/j.cell.2013.07.004.
13. Clevers H. Stem cells: a unifying theory for the crypt. Nature 2013, 495(7439):53-54. 10.1038/nature11958.
14. Gerbe F., van Es J.H., Makrini L., et al. Distinct ATOH1 and Neurog3 requirements define tuft cells as a new secretory cell type in the intestinal epithelium. J Cell Biol 2011, 192(5):767-780. 10.1083/jcb.201010127.
15. Gomez D., Shankman L.S., Nguyen A.T., Owens G.K. Detection of histone modifications at specific gene loci in single cells in histological sections. Nat Methods 2013, 10(2):171-177. 10.1038/nmeth.2332.
16. Gratchev A., Siedow A., Bumke-Vogt C., et al. Regulation of the intestinal mucin MUC2 gene expression in vivo: evidence for the role of promoter methylation. Cancer Lett 2001, 168(1):71-80. (Available at: http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=PubMed&dopt=Citation&list_uids=11368880).
17. Grossmann J., Walther K., Artinger M., Rümmele P., Woenckhaus M., Schölmerich J. Induction of apoptosis before shedding of human intestinal epithelial cells. Am J Gastroenterol 2002, 97(6):1421-1428. 10.1111/j.1572-0241.2002.05787.x.
18. Ho L.-L., Sinha A., Verzi M., Bernt K.M., Armstrong S.A., Shivdasani R.A. DOT1L-mediated H3K79 methylation in chromatin is dispensable for Wnt pathway-specific and other intestinal epithelial functions. Mol Cell Biol 2013, 33(9):1735-1745. 10.1128/MCB. 01463-12.
19. Itzkovitz S., Lyubimova A., Blat I.C., et al. Single-molecule transcript counting of stem-cell markers in the mouse intestine. Nat Cell Biol 2012, 14(1):106-114. 10.1038/ncb2384.
20. Kaaij L.T., van de Wetering M., Fang F., et al. DNA methylation dynamics during intestinal stem cell differentiation reveals enhancers driving gene expression in the villus. Genome Biol 2013, 14(5):R50. 10.1186/gb-2013-14-5-r50.
21. Kawai H., Tomii K., Toyooka S., et al. Promoter methylation downregulates CDX2 expression in colorectal carcinomas. Oncol Rep 2005, 13(3):547-551. (Available at: http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=PubMed&dopt=Citation&list_uids=15706431).
22. Kent W.J., Sugnet C.W., Furey T.S., et al. The human genome browser at UCSC. Genome Res 2002, 12(6):996-1006. (Article published online before print in May 2002). 10.1101/gr.229102.
23. Kim T.-H., Li F., Ferreiro-Neira I., et al. Broadly permissive intestinal chromatin underlies lateral inhibition and cell plasticity. Nature 2014, 506(7489):511-515. 10.1038/nature12903.
24. Kwon O.-H., Park J.-L., Baek S.-J., et al. Aberrant upregulation of ASCL2 by promoter demethylation promotes the growth and resistance to 5-fluorouracil of gastric cancer cells. Cancer Sci 2013, 104(3):391-397. 10.1111/cas.12076.
25. Li L.-C., Dahiya R. MethPrimer: designing primers for methylation PCRs. Bioinformatics 2002, 18(11):1427-1431. (Available at: http://www.ncbi.nlm.nih.gov/pubmed/12424112. Accessed September 3, 2014).
26. Loh Y.H., Zhang W., Chen X., George J., Ng H.H. Jmjd1a and Jmjd2c histone H3 Lys 9 demethylases regulate self-renewal in embryonic stem cells. Genes Dev 2007, 21(20):2545-2557. (21/20/2545 [pii]). 10.1101/gad.1588207.
27. Miranda T.B., Jones P.A. DNA methylation: the nuts and bolts of repression. J Cell Physiol 2007, 213(2):384-390. 10.1002/jcp.21224.
28. Mori-Akiyama Y., van den Born M., van Es J.H., et al. SOX9 is required for the differentiation of Paneth cells in the intestinal epithelium. Gastroenterology 2007, 133(2):539-546. (Available at: http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=PubMed&dopt=Citation&list_uids=17681175).
29. Oguro H., Yuan J., Ichikawa H., et al. Poised lineage specification in multipotential hematopoietic stem and progenitor cells by the polycomb protein Bmi1. Cell Stem Cell 2010, 6(3):279-286. 10.1016/j.stem.2010.01.005.
30. Pennarossa G., Maffei S., Campagnol M., Tarantini L., Gandolfi F., Brevini T.A.L. Brief demethylation step allows the conversion of adult human skin fibroblasts into insulin-secreting cells. Proc Natl Acad Sci U S A 2013, 110(22):8948-8953. 10.1073/pnas.1220637110.
31. Ramalingam S., Daughtridge G.W., Johnston M.J., Gracz A.D., Magness S.T. Distinct levels of Sox9 expression mark colon epithelial stem cells that form colonoids in culture. Am J Physiol Gastrointest Liver Physiol 2012, 302(1):G10-G20. 10.1152/ajpgi.00277.2011.
32. Rodriguez J., Muñoz M., Vives L., Frangou C.G., Groudine M., Peinado M.A. Bivalent domains enforce transcriptional memory of DNA methylated genes in cancer cells. Proc Natl Acad Sci U S A 2008, 105(50):19809-19814. 10.1073/pnas.0810133105.
33. Sangiorgi E., Capecchi M.R. Bmi1 is expressed in vivo in intestinal stem cells. Nat Genet 2008, 40(7):915-920. (ng.165 [pii]). 10.1038/ng.165.
34. Scoville D.H., Sato T., He X.C., Li L. Current view: intestinal stem cells and signaling. Gastroenterology 2008, 134(3):849-864. (S0016-5085(08)00185-6 [pii]). 10.1053/j.gastro.2008.01.079.
35. Sheaffer K.L., Kim R., Aoki R., et al. DNA methylation is required for the control of stem cell differentiation in the small intestine. Genes Dev 2014, 28(6):652-664. 10.1101/gad.230318.113.
36. Shen X., Liu Y., Hsu Y.J., et al. EZH1 mediates methylation on histone H3 lysine 27 and complements EZH2 in maintaining stem cell identity and executing pluripotency. Mol Cell 2008, 32(4):491-502. (S1097-2765(08)00732-6 [pii]). 10.1016/j.molcel.2008.10.016.
37. Tollervey J.R., Lunyak V.V. Epigenetics: judge, jury and executioner of stem cell fate. Epigenetics 2012, 7(8):823-840. 10.4161/epi.21141.
38. Tytgat K.M., Buller H.A., Opdam F.J., Kim Y.S., Einerhand A.W., Dekker J. Biosynthesis of human colonic mucin: Muc2 is the prominent secretory mucin. Gastroenterology 1994, 107(5):1352-1363. (doi: S0016508594003318 [pii]).
39. Verzi M.P., Shin H., San Roman A.K., Liu X.S., Shivdasani R.A. Intestinal master transcription factor CDX2 controls chromatin access for partner transcription factor binding. Mol Cell Biol 2013, 33(2):281-292. 10.1128/MCB. 01185-12.
40. Vincent A., Van Seuningen I. Epigenetics, stem cells and epithelial cell fate. Differentiation 2009, 78(2-3):99-107. (S0301-4681(09)00083-8 [pii]). 10.1016/j.diff.2009.07.002.
41. Vincent A., Van Seuningen I. On the epigenetic origin of cancer stem cells. Biochim Biophys Acta 2012, 1826(1):83-88. (S0304-419X(12)00023-6 [pii]). 10.1016/j.bbcan.2012.03.009.
42. Vincent A., Omura N., Hong S.-M., Jaffe A., Eshleman J., Goggins M. Genome-wide analysis of promoter methylation associated with gene expression profile in pancreatic adenocarcinoma. Clin Cancer Res 2011, 17(13):4341-4354.
43. Wang F., Scoville D., He X.C., et al. Isolation and characterization of intestinal stem cells based on surface marker combinations and colony-formation assay. Gastroenterology 2013, 145(2):383-395.e1-21. 10.1053/j.gastro.2013.04.050.