High resolution methylome analysis reveals widespread functional hypomethylation during adult human erythropoiesis

Journal of Biological Chemistry

Volumn 288, Issue 13, 2013, Pages 8805-8814

  Yu, Yiting ^a   Mo, Yongkai ^a   Ebenezer, David ^b   Bhattacharyya, Sanchari ^a   Liu, Hui ^b   Sundaravel, Sriram ^b   Giricz, Orsolya ^a   Wontakal, Sandeep ^a   Cartier, Jessy ^a   Caces, Bennett ^b   Artz, Andrew ^b   Nischal, Sangeeta ^a   Bhagat, Tushar ^a   Bathon, Kathleen ^a   Maqbool, Shahina ^a   Gligich, Oleg ^a   Suzuki, Masako ^a   Steidl, Ulrich ^a   Godley, Lucy ^b   Skoultchi, Art ^a   Greally, John ^a   Wickrema, Amittha ^b   Verma, Amit ^a   more..

^a ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

^b UNIVERSITY OF CHICAGO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COMPREHENSIVE ANALYSIS; ERYTHROCYTE MEMBRANE; ERYTHROID DIFFERENTIATION; HEMATOPOIETIC STEM CELLS; INTEGRATIVE ANALYSIS; REGULATORY MECHANISM; TERMINAL DEVELOPMENT; TRANSCRIPTION FACTOR BINDING SITES;

ALKYLATION; BINDING SITES; CELL MEMBRANES; GENE ENCODING; NETWORK CODING; TRANSCRIPTION FACTORS;

BLOOD;

PROTEIN MYB; TRANSCRIPTION FACTOR GATA; TRANSCRIPTION FACTOR GATA 1; TRANSCRIPTION FACTOR TAL1;

ARTICLE; BINDING SITE; CELL DIFFERENTIATION; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; CPG ISLAND; DNA METHYLATION; EPIGENETICS; ERYTHROPOIESIS; GENE EXPRESSION; HUMAN; HUMAN CELL; INTRON; PRIORITY JOURNAL; PROMOTER REGION; QUANTITATIVE ANALYSIS; REGULATORY MECHANISM; TRANSCRIPTION FACTOR GATA 1 GENE;

ANTIGENS, CD34; BINDING SITES; CELL DIFFERENTIATION; CPG ISLANDS; DNA METHYLATION; EPIGENESIS, GENETIC; EPIGENOMICS; ERYTHROCYTES; ERYTHROPOIESIS; FLOW CYTOMETRY; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENOME, HUMAN; GENOMICS; HUMANS; INTRONS; METHYLATION; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; STEM CELLS;

EID: 84875974292     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.423756     Document Type: Article

References (26)

1. Esteller, M. (2003) Cancer epigenetics. DNA methylation and chromatin alterations in human cancer. Adv. Exp. Med. Biol. 532, 39-49
2. Figueroa, M. E., Lugthart, S., Li, Y., Erpelinck-Verschueren, C., Deng, X., Christos, P. J., Schifano, E., Booth, J., van Putten, W., Skrabanek, L., Campagne, F., Mazumdar, M., Greally, J. M., Valk, P. J., Löwenberg, B., Delwel, R., and Melnick, A. (2010) DNA methylation signatures identify biologically distinct subtypes in acute myeloid leukemia. Cancer Cell 17, 13-27
3. Khulan, B., Thompson, R. F., Ye, K., Fazzari, M. J., Suzuki, M., Stasiek, E., Figueroa, M. E., Glass, J. L., Chen, Q., Montagna, C., Hatchwell, E., Selzer, R. R., Richmond, T. A., Green, R. D., Melnick, A., and Greally, J. M. (2006) Comparative isoschizomer profiling of cytosine methylation. The HELP assay. Genome Res. 16, 1046-1055
4. Thompson, R. F., Reimers, M., Khulan, B., Gissot, M., Richmond, T. A., Chen, Q., Zheng, X., Kim, K., and Greally, J. M. (2008) An analytical pipeline for genomic representations used for cytosine methylation studies. Bioinformatics 24, 1161-1167
5. Arai, E., and Kanai, Y. (2010) Genetic and epigenetic alterations during renal carcinogenesis. Int. J. Clin. Exp. Pathol. 4, 58-73
6. Baldewijns, M. M., van Vlodrop, I. J., Schouten, L. J., Soetekouw, P. M., de Bruïne, A. P., and van Engeland, M. (2008) Genetics and epigenetics of renal cell cancer. Biochim. Biophys. Acta 1785, 133-155
7. Irizarry, R. A., Ladd-Acosta, C., Wen, B., Wu, Z., Montano, C., Onyango, P., Cui, H., Gabo, K., Rongione, M., Webster, M., Ji, H., Potash, J. B., Sabunciyan, S., and Feinberg, A. P. (2009) The human colon cancer methylome shows similar hypo- and hypermethylation at conserved tissue- specific CpG island shores. Nat. Genet. 41, 178-186
8. Ball, M. P., Li, J. B., Gao, Y., Lee, J. H., LeProust, E. M., Park, I. H., Xie, B., Daley, G. Q., and Church, G. M. (2009) Targeted and genome-scale strategies reveal gene-body methylation signatures in human cells. Nat. Biotechnol. 27, 361-368
9. Alvarez, H., Opalinska, J., Zhou, L., Sohal, D., Fazzari, M. J., Yu, Y., Montagna, C., Montgomery, E. A., Canto, M., Dunbar, K. B., Wang, J., Roa, J. C., Mo, Y., Bhagat, T., Ramesh, K. H., Cannizzaro, L., Mollenhauer, J., Thompson, R. F., Suzuki, M., Meltzer, S., Melnick, A., Greally, J. M., Maitra, A., and Verma, A. (2011) Widespread hypomethylation occurs early and synergizes with gene amplification during esophageal carcinogenesis. PLoS Genet. 7, e1001356
10. Oda, M., Glass, J. L., Thompson, R. F., Mo, Y., Olivier, E. N., Figueroa, M. E., Selzer, R. R., Richmond, T. A., Zhang, X., Dannenberg, L., Green, R. D., Melnick, A., Hatchwell, E., Bouhassira, E. E., Verma, A., Suzuki, M., and Greally, J. M. (2009) High-resolution genome-wide cytosine methylation profiling with simultaneous copy number analysis and optimization for limited cell numbers. Nucleic Acids Res. 37, 3829-3839
11. Figueroa, M. E., Reimers, M., Thompson, R. F., Ye, K., Li, Y., Selzer, R. R., Fridriksson, J., Paietta, E., Wiernik, P., Green, R. D., Greally, J. M., and Melnick, A. (2008) An integrative genomic and epigenomic approach for the study of transcriptional regulation. PloS One 3, e1882
12. Figueroa, M. E., Wouters, B. J., Skrabanek, L., Glass, J., Li, Y., Erpelinck-Verschueren, C. A., Langerak, A. W., Löwenberg, B., Fazzari, M., Greally, J. M., Valk, P. J., Melnick, A., and Delwel, R. (2009) Genome-wide epigenetic analysis delineates a biologically distinct immature acute leukemia with myeloid/T-lymphoid features. Blood 113, 2795-2804
13. Heinz, S., Benner, C., Spann, N., Bertolino, E., Lin, Y. C., Laslo, P., Cheng, J. X., Murre, C., Singh, H., and Glass, C. K. (2010) Simple combinations of lineage-determining transcription factors prime cis-regulatory elements required for macrophage and B cell identities. Mol. Cell 38, 576-589
14. Wontakal, S. N., Guo, X., Will, B., Shi, M., Raha, D., Mahajan, M. C., Weissman, S., Snyder, M., Steidl, U., Zheng, D., and Skoultchi, A. I. (2011) A large gene network in immature erythroid cells is controlled by the myeloid and B cell transcriptional regulator PU.1. PLoS Genet. 7, e1001392
15. Wickrema, A., and Crispino, J. D. (2007) Erythroid and megakaryocytic transformation. Oncogene 26, 6803-6815
16. Yamamoto, M. L., Clark, T. A., Gee, S. L., Kang, J. A., Schweitzer, A. C., Wickrema, A., and Conboy, J. G. (2009) Alternative pre-mRNA splicing switches modulate gene expression in late erythropoiesis. Blood 113, 3363-3370
17. Kang, J. A., Zhou, Y., Weis, T. L., Liu, H., Ulaszek, J., Satgurunathan, N., Zhou, L., van Besien, K., Crispino, J., Verma, A., Low, P. S., and Wickrema, A. (2008) Osteopontin regulates actin cytoskeleton and contributes to cell proliferation in primary erythroblasts. J. Biol. Chem. 283, 6997-7006
18. Uddin, S., Ah-Kang, J., Ulaszek, J., Mahmud, D., and Wickrema, A. (2004) Differentiation stage-specific activation of p38 mitogen-activated protein kinase isoforms in primary human erythroid cells. Proc. Natl. Acad. Sci. U.S.A. 101, 147-152
19. Wontakal, S. N., Guo, X., Smith, C., MacCarthy, T., Bresnick, E. H., Bergman, A., Snyder, M. P., Weissman, S. M., Zheng, D., and Skoultchi, A. I. (2012) A core erythroid transcriptional network is repressed by a master regulator of myelo-lymphoid differentiation. Proc. Natl. Acad. Sci. U.S.A. 109, 3832-3837
20. Rekhtman, N., Choe, K. S., Matushansky, I., Murray, S., Stopka, T., and Skoultchi, A. I. (2003) PU.1 and pRB interact and cooperate to repress GATA-1 and block erythroid differentiation. Mol. Cell. Biol. 23, 7460-7474
21. Stopka, T., Amanatullah, D. F., Papetti, M., and Skoultchi, A. I. (2005) PU.1 inhibits the erythroid program by binding to GATA-1 on DNA and creating a repressive chromatin structure. EMBO J. 24, 3712-3723
22. Shearstone, J. R., Pop, R., Bock, C., Boyle, P., Meissner, A., and Socolovsky, M. (2011) Global DNA demethylation during mouse erythropoiesis in vivo. Science 334, 799-802
23. Ji, H., Ehrlich, L. I., Seita, J., Murakami, P., Doi, A., Lindau, P., Lee, H., Aryee, M. J., Irizarry, R. A., Kim, K., Rossi, D. J., Inlay, M. A., Serwold, T., Karsunky, H., Ho, L., Daley, G. Q., Weissman, I. L., and Feinberg, A. P. (2010) Comprehensive methylome map of lineage commitment from haematopoietic progenitors. Nature 467, 338-342
24. Trowbridge, J. J., Snow, J. W., Kim, J., and Orkin, S. H. (2009) DNA methyltransferase 1 is essential for and uniquely regulates hematopoietic stem and progenitor cells. Cell Stem Cell 5, 442-449
25. Suzuki, M., Yamada, T., Kihara-Negishi, F., Sakurai, T., Hara, E., Tenen, D. G., Hozumi, N., and Oikawa, T. (2006) Site-specific DNA methylation by a complex of PU.1 and Dnmt3a/b. Oncogene 25, 2477-2488
26. Seshasayee, D., Geiger, J. N., Gaines, P., and Wojchowski, D. M. (2000) Intron 1 elements promote erythroid-specific GATA-1 gene expression. J. Biol. Chem. 275, 22969-22977