Dnmt1 is essential to maintain progenitors in the perinatal intestinal epithelium

Development (Cambridge)

Volumn 142, Issue 12, 2015, Pages 2163-2172

  Elliott, Ellen N ^a   Sheaffer, Karyn L ^a   Schug, Jonathan ^a   Stappenbeck, Thaddeus S ^b   Kaestner, Klaus H ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

DNA damage response; DNA methylation; Intestinal epithelial development

Indexed keywords

ATM PROTEIN; CHECKPOINT KINASE 2; DNA METHYLTRANSFERASE 1; DNA METHYLTRANSFERASE 3A; DNA METHYLTRANSFERASE 3B; MESSENGER RNA; PROTEIN MLH1; PROTEIN P21; DNA (CYTOSINE 5) METHYLTRANSFERASE; DNA (CYTOSINE-5-)-METHYLTRANSFERASE 1;

ADULT; ANIMAL EXPERIMENT; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL CYCLE ARREST; CELL DIFFERENTIATION; CELL PROLIFERATION; CONTROLLED STUDY; DNA DAMAGE; DNA METHYLATION; DNA REPLICATION; DOUBLE STRANDED DNA BREAK; EMBRYO; GENE EXPRESSION; GENOMIC INSTABILITY; IN VITRO STUDY; INTESTINAL STEM CELL; INTESTINE CRYPT; INTESTINE EPITHELIUM; LOXP SITE; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PERINATAL DEVELOPMENT; PRIORITY JOURNAL; PROTEIN LOCALIZATION; RNA SEQUENCE; ANIMAL; CYTOLOGY; EMBRYOLOGY; GENE EXPRESSION REGULATION; GENETICS; INTESTINE MUCOSA; KNOCKOUT MOUSE; MOLECULAR GENETICS; ORGANOGENESIS; PHYSIOLOGY; STEM CELL;

ANIMALS; APOPTOSIS; CELL PROLIFERATION; DNA (CYTOSINE-5-)-METHYLTRANSFERASE; DNA DAMAGE; DNA METHYLATION; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENOMIC INSTABILITY; INTESTINAL MUCOSA; MICE; MICE, KNOCKOUT; MOLECULAR SEQUENCE DATA; ORGANOGENESIS; STEM CELLS;

EID: 84931056085     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.117341     Document Type: Article

References (45)

1. Ahuja, N., Mohan, A. L., Li, Q., Stolker, J. M., Herman, J. G., Hamilton, S. R., Baylin, S. B. and Issa, J. P. (1997). Association between CpG island methylation and microsatellite instability in colorectal cancer. Cancer Res. 57, 3370-3374
2. Allan, L. A., Duhig, T., Read, M. and Fried, M. (2000). The p21(WAF1/CIP1) promoter is methylated in Rat-1 cells: stable restoration of p53-dependent p21 (WAF1/CIP1) expression after transfection of a genomic clone containing the p21 (WAF1/CIP1) gene. Mol. Cell. Biol. 20, 1291-1298
3. Al-Nafussi, A. I. and Wright, N. A. (1982). Cell kinetics in the mouse small intestine during immediate postnatal life. Virchows Arch. B Cell Pathol. Incl. Mol. Pathol. 40, 51-62
4. Ashburner, M., Ball, C. A., Blake, J. A., Botstein, D., Butler, H., Cherry, J.M., Davis, A. P., Dolinski, K., Dwight, S. S., Eppig, J. T. et al. (2000). Gene ontology: tool for the unification of biology. The Gene Ontology Consortium. Nat. Genet. 25, 25-29
5. Baubonis, W. and Sauer, B. (1993). Genomic targeting with purified Cre recombinase. Nucleic Acids Res. 21, 2025-2029
6. Bevins, C. L. and Salzman, N. H. (2011). Paneth cells, antimicrobial peptides and maintenance of intestinal homeostasis. Nat. Rev. Microbiol. 9, 356-368
7. Brenner, C., Deplus, R., Didelot, C., Loriot, A., Viré E., DeSmet, C., Gutierrez, A., Danovi D., Bernard D., Boon T. et al. (2005). Myc represses transcription through recruitment of DNA methyltransferase corepressor. EMBO J. 24, 336-346
8. Bry, L., Falk, P., Huttner, K., Ouellette, A., Midtvedt, T. and Gordon, J. I. (1994). Paneth cell differentiation in the developing intestine of normal and transgenic mice. Proc. Natl. Acad. Sci. USA 91, 10335-10339
9. Bunz, F., Dutriaux, A., Lengauer, C., Waldman, T., Zhou, S., Brown, J. P., Sedivy, J. M., Kinzler, K.W. and Vogelstein, B. (1998). Requirement for p53 and p21 to sustain G2 arrest after DNA damage. Science 282, 1497-1501
10. Chang, B.-D., Watanabe, K., Broude, E. V., Fang, J., Poole, J. C., Kalinichenko, T. V. and Roninson, I. B. (2000). Effects of p21Waf1/Cip1/Sdi1 on cellular gene expression: implications for carcinogenesis, senescence, and age-related diseases. Proc. Natl. Acad. Sci. USA 97, 4291-4296
11. Chen, R. Z., Pettersson, U., Beard, C., Jackson-Grusby, L. and Jaenisch, R. (1998). DNA hypomethylation leads to elevated mutation rates. Nature 395, 89-93
12. Chen, T., Hevi, S., Gay, F., Tsujimoto, N., He, T., Zhang, B., Ueda, Y. and Li, E. (2007). Complete inactivation of DNMT1 leads to mitotic catastrophe in human cancer cells. Nat. Genet. 39, 391-396
13. Chen, P.-Y., Cokus, S. J. and Pellegrini, M. (2010). BS Seeker: precise mapping for bisulfite sequencing. BMC Bioinformatics 11, 203
14. Deng, C., Zhang, P., Harper, J. W., Elledge, S. J. and Leder, P. (1995). Mice lacking p21CIP1/WAF1 undergo normal development, but are defective in G1 checkpoint control. Cell 82, 675-684
15. Edgar, R., Domrachev, M. and Lash, A. E. (2002). Gene expression omnibus: NCBI gene expression and hybridization array data repository. Nucleic Acids Res. 30, 207-210
16. El Marjou, F., Janssen, K.-P., Chang, B. H.-J., Li, M., Hindie, V., Chan, L., Louvard, D., Chambon, P., Metzger, D. and Robine, S. (2004). Tissue-specific and inducible Cre-mediated recombination in the gut epithelium. Genesis 39, 186-193
17. Fan, G., Beard, C., Chen, R. Z., Csankovszki, G., Sun, Y., Siniaia, M., Biniszkiewicz, D., Bates, B., Lee, P. P., Kuhn, R. et al. (2001). DNA hypomethylation perturbs the function and survival of CNS neurons in postnatal animals. J. Neurosci. 21, 788-797
18. Fordham, R. P., Yui, S., Hannan, N. R. F., Soendergaard, C., Madgwick, A., Schweiger, P. J., Nielsen, O. H., Vallier, L., Pedersen, R. A., Nakamura, T. et al. (2013). Transplantation of expanded fetal intestinal progenitors contributes to colon regeneration after injury. Cell Stem Cell 13, 734-744
19. Georgia, S., Kanji, M. and Bhushan, A. (2013). DNMT1 represses p53 to maintain progenitor cell survival during pancreatic organogenesis. Genes Dev. 27, 372-377
20. Gupta, R. K., Gao, N., Gorski, R. K., White, P., Hardy, O. T., Rafiq, K., Brestelli, J. E., Chen, G., Stoeckert, C. J. and Kaestner, K. H. (2007). Expansion of adult beta-cell mass in response to increased metabolic demand is dependent on HNF- 4alpha. Genes Dev. 21, 756-769
21. Hall, P. A., Coates, P. J., Ansari, B. and Hopwood, D. (1994). Regulation of cell number in the mammalian gastrointestinal tract: the importance of apoptosis. J. Cell Sci. 107, 3569-3577
22. Itzkovitz, S., Blat, I. C., Jacks, T., Clevers, H. and van Oudenaarden, A. (2012). Optimality in the development of intestinal crypts. Cell 148, 608-619
23. Jackson-Grusby, L., Beard, C., Possemato, R., Tudor, M., Fambrough, D., Csankovszki, G., Dausman, J., Lee, P., Wilson, C., Lander, E. et al. (2001). Loss of genomic methylation causes p53-dependent apoptosis and epigenetic deregulation. Nat. Genet. 27, 31-39
24. Jones, P. A. and Takai, D. (2001). The role of DNA methylation in mammalian epigenetics. Science 293, 1068-1070
25. Knox, J. D., Araujo, F. D., Bigey, P., Slack, A. D., Price, G. B., Zannis- Hadjopoulos, M. and Szyf, M. (2000). Inhibition of DNA methyltransferase inhibits DNA replication. J. Biol. Chem. 275, 17986-17990
26. Lane, N., Dean, W., Erhardt, S., Hajkova, P., Surani, A., Walter, J. and Reik, W. (2003). Resistance of IAPs to methylation reprogramming may provide a mechanism for epigenetic inheritance in the mouse. Genesis 35, 88-93
27. Li, E., Bestor, T. H. and Jaenisch, R. (1992). Targeted mutation of the DNA methyltransferase gene results in embryonic lethality. Cell 69, 915-926
28. Long, M. A. and Rossi, F. M. V. (2009). Silencing inhibits Cre-mediated recombination of the Z/AP and Z/EG reporters in adult cells. PLoS ONE 4, e5435
29. Loughery, J. E. P., Dunne, P. D., O’Neill, K. M., Meehan, R. R., McDaid, J. R. and Walsh, C. P. (2011). DNMT1 deficiency triggers mismatch repair defects in human cells through depletion of repair protein levels in a process involving the DNA damage response. Hum. Mol. Genet. 20, 3241-3255
30. Madison, B. B., Dunbar, L., Qiao, X. T., Braunstein, K., Braunstein, E. and Gumucio, D. L. (2002). 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. 277, 33275-33283
31. Miyoshi, H., Ajima, R., Luo, C. T., Yamaguchi, T. P. and Stappenbeck, T. S. (2012). Wnt5a potentiates TGF-β signaling to promote colonic crypt regeneration after tissue injury. Science 338, 108-113
32. Mortusewicz, O., Schermelleh, L., Walter, J., Cardoso, M. C. and Leonhardt, H. (2005). Recruitment of DNA methyltransferase I to DNA repair sites. Proc. Natl. Acad. Sci. USA 102, 8905-8909
33. Mustata, R. C., Vasile, G., Fernandez-Vallone, V., Strollo, S., Lefort, A., Libert, F., Monteyne, D., Pérez-Morga, D., Vassart, G. and Garcia, M.-I. (2013). Identification of Lgr5-independent spheroid-generating progenitors of the mouse fetal intestinal epithelium. Cell Rep. 5, 421-432
34. Samuel, M. S., Suzuki, H., Buchert, M., Putoczki, T. L., Tebbutt, N. C., Lundgren- May, T., Christou, A., Inglese, M., Toyota, M., Heath, J. K. et al. (2009). Elevated Dnmt3a activity promotes polyposis in Apc(Min) mice by relaxing extracellular restraints on Wnt signaling. Gastroenterology 137, 902-913.e11
35. Sato, T., Vries, R. G., Snippert, H. J., van de Wetering, M., Barker, N., Stange, D. E., van Es, J. H., Abo, A., Kujala, P., Peters, P. J. et al. (2009). Single Lgr5 stem cells build crypt-villus structures in vitro without a mesenchymal niche. Nature 459, 262-265
36. Schneider, C. A., Rasband, W. S. and Eliceiri, K.W. (2012). NIH Image to ImageJ: 25 years of image analysis. Nat. Methods 9, 671-675
37. Sheaffer, K. L., Kim, R., Aoki, R., Elliott, E. N., Schug, J., Burger, L., Schübeler, D. and Kaestner, K. H. (2014). DNA methylation is required for the control of stem cell differentiation in the small intestine. Genes Dev. 28, 652-664
38. Trapnell, C., Roberts, A., Goff, L., Pertea, G., Kim, D., Kelley, D. R., Pimentel, H., Salzberg, S. L., Rinn, J. L. and Pachter, L. (2012). Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks. Nat. Protoc. 7, 562-578
39. Tremblay, K. D., Saam, J. R., Ingram, R. S., Tilghman, S. M. and Bartolomei, M. S. (1995). A paternal-specific methylation imprint marks the alleles of the mouse H19 gene. Nat. Genet. 9, 407-413
40. Unterberger, A., Andrews, S. D., Weaver, I. C. G. and Szyf, M. (2006). DNA methyltransferase 1 knockdown activates a replication stress checkpoint. Mol. Cell. Biol. 26, 7575-7586
41. van deWetering, M., Sancho, E., Verweij, C., de Lau, W., Oving, I., Hurlstone, A., van der Horn, K., Batlle, E., Coudreuse, D., Haramis, A.-P. et al. (2002). The beta-catenin/TCF-4 complex imposes a crypt progenitor phenotype on colorectal cancer cells. Cell 111, 241-250
42. Vandesompele, J., De Preter, K., Pattyn, F., Poppe, B., Van Roy, N., De Paepe, A. and Speleman, F. (2002). Accurate normalization of real-time quantitative RTPCR data by geometric averaging of multiple internal control genes. Genome Biol. 3, research0034-research0034.11
43. Waterston, R. H., Lindblad-Toh, K., Birney, E., Rogers, J., Abril, J. F., Agarwal, P., Agarwala, R., Ainscough, R., Alexandersson, M., An, P. et al. (2002). Initial sequencing and comparative analysis of the mouse genome. Nature 420, 520-562
44. Yang, A. S., Estécio, M. R. H., Doshi, K., Kondo, Y., Tajara, E. H. and Issa, J.-P. J. (2004). A simple method for estimating global DNA methylation using bisulfite PCR of repetitive DNA elements. Nucleic Acids Res. 32, e38
45. Zhu, W.-G., Srinivasan, K., Dai, Z., Duan, W., Druhan, L. J., Ding, H., Yee, L., Villalona-Calero, M. A., Plass, C. and Otterson, G. A. (2003). Methylation of adjacent CpG sites affects Sp1/Sp3 binding and activity in the p21(Cip1) promoter. Mol. Cell. Biol. 23, 4056-4065.