Preferential binding of HIF-1 to transcriptionally active loci determines cell-type specific response to hypoxia

Genome Biology

Volumn 10, Issue 10, 2009, Pages

  Xia, Xiaobo ^a   Kung, Andrew L ^a  

^a BOSTON CHILDREN S HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HISTONE H3; HISTONE H3K4; HYPOXIA INDUCIBLE FACTOR 1; MESSENGER RNA; RNA POLYMERASE II; UNCLASSIFIED DRUG;

ARTICLE; CANCER CELL CULTURE; CELL HYPOXIA; CELL SPECIFICITY; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; DNA METHYLATION; EPIGENETICS; GENE EXPRESSION PROFILING; GENE INDUCTION; GENE REPRESSION; GLIOMA CELL; HEPATOMA CELL; HUMAN; HUMAN CELL; PROTEIN BINDING; TRANSACTIVATION; ANTIBODY SPECIFICITY; BIOLOGICAL MODEL; GENE EXPRESSION REGULATION; GENE LOCUS; GENETIC TRANSCRIPTION; GENETICS; METABOLISM; PROMOTER REGION; TUMOR CELL LINE;

CELL HYPOXIA; CELL LINE, TUMOR; GENE EXPRESSION REGULATION; GENETIC LOCI; HUMANS; HYPOXIA-INDUCIBLE FACTOR 1; MODELS, GENETIC; ORGAN SPECIFICITY; PROMOTER REGIONS, GENETIC; PROTEIN BINDING; TRANSCRIPTION, GENETIC;

EID: 75349114759     PISSN: 14747596     EISSN: 1474760X     Source Type: Journal    
DOI: 10.1186/gb-2009-10-10-r113     Document Type: Article

References (36)

1. Semenza GL. Targeting HIF-1 for cancer therapy. Nat Rev Cancer 2003, 3:721-732. 10.1038/nrc1187, 13130303.
2. Xia X, Lemieux ME, Li W, Carroll JS, Brown M, Liu XS, Kung AL. Integrative analysis of HIF binding and transactivation reveals its role in maintaining histone methylation homeostasis. Proc Natl Acad Sci USA 2009, 106:4260-4265. 10.1073/pnas.0810067106, 2657396, 19255431.
3. Wenger RH, Stiehl DP, Camenisch G. Integration of oxygen signaling at the consensus HRE. Sci STKE 2005, 2005:re12. 10.1126/stke.3062005re12, 16234508.
4. Mole DR, Blancher C, Copley RR, Pollard PJ, Gleadle JM, Ragoussis J, Ratcliffe PJ. Genome-wide association of HIF-1alpha and HIF-2alpha DNA-binding with expression profiling of hypoxia inducible transcripts. J Biol Chem 2009, 284:16767-16775. 10.1074/jbc.M901790200, 2719312, 19386601.
5. Carroll JS, Liu XS, Brodsky AS, Li W, Meyer CA, Szary AJ, Eeckhoute J, Shao W, Hestermann EV, Geistlinger TR, Fox EA, Silver PA, Brown M. Chromosome-wide mapping of estrogen receptor binding reveals long-range regulation requiring the forkhead protein FoxA1. Cell 2005, 122:33-43. 10.1016/j.cell.2005.05.008, 16009131.
6. Bieda M, Xu X, Singer MA, Green R, Farnham PJ. Unbiased location analysis of E2F1-binding sites suggests a widespread role for E2F1 in the human genome. Genome Res 2006, 16:595-605. 10.1101/gr.4887606, 1457046, 16606705.
7. Yang A, Zhu Z, Kapranov P, McKeon F, Church GM, Gingeras TR, Struhl K. Relationships between p63 binding, DNA sequence, transcription activity, and biological function in human cells. Mol Cell 2006, 24:593-602. 10.1016/j.molcel.2006.10.018, 17188034.
8. Lupien M, Eeckhoute J, Meyer CA, Wang Q, Zhang Y, Li W, Carroll JS, Liu XS, Brown M. FoxA1 translates epigenetic signatures into enhancer-driven lineage-specific transcription. Cell 2008, 132:958-970. 10.1016/j.cell.2008.01.018, 2323438, 18358809.
9. Iguchi-Ariga SM, Schaffner W. CpG methylation of the cAMP-responsive enhancer/promoter sequence TGACGTCA abolishes specific factor binding as well as transcriptional activation. Genes Dev 1989, 3:612-619. 10.1101/gad.3.5.612, 2545524.
10. Perini G, Diolaiti D, Porro A, Della Valle G. In vivo transcriptional regulation of N-Myc target genes is controlled by E-box methylation. Proc Natl Acad Sci USA 2005, 102:12117-12122. 10.1073/pnas.0409097102, 1184034,1184034, 16093321.
11. Wenger RH, Kvietikova I, Rolfs A, Camenisch G, Gassmann M. Oxygen-regulated erythropoietin gene expression is dependent on a CpG methylation-free hypoxia-inducible factor-1 DNA-binding site. Eur J Biochem 1998, 253:771-777. 10.1046/j.1432-1327.1998.2530771.x, 9654078.
12. Rossler J, Stolze I, Frede S, Freitag P, Schweigerer L, Havers W, Fandrey J. Hypoxia-induced erythropoietin expression in human neuroblastoma requires a methylation free HIF-1 binding site. J Cell Biochem 2004, 93:153-161. 10.1002/jcb.20133, 15352172.
13. Bacon AL, Fox S, Turley H, Harris AL. Selective silencing of the hypoxia-inducible factor 1 target gene BNIP3 by histone deacetylation and methylation in colorectal cancer. Oncogene 2007, 26:132-141. 10.1038/sj.onc.1209761, 16799636.
14. Hu CJ, Wang LY, Chodosh LA, Keith B, Simon MC. Differential roles of hypoxia-inducible factor 1alpha (HIF-1alpha) and HIF-2alpha in hypoxic gene regulation. Mol Cell Biol 2003, 23:9361-9374. 10.1128/MCB.23.24.9361-9374.2003, 309606, 14645546.
15. Vengellur A, Woods BG, Ryan HE, Johnson RS, LaPres JJ. Gene expression profiling of the hypoxia signaling pathway in hypoxia-inducible factor 1alpha null mouse embryonic fibroblasts. Gene Expr 2003, 11:181-197. 10.3727/000000003108749062, 14686790.
16. Greijer AE, Groep P, Kemming D, Shvarts A, Semenza GL, Meijer GA, Wiel MA, Belien JA, van Diest PJ, Wall E. Up-regulation of gene expression by hypoxia is mediated predominantly by hypoxia-inducible factor 1 (HIF-1). J Pathol 2005, 206:291-304. 10.1002/path.1778, 15906272.
17. Chi JT, Wang Z, Nuyten DS, Rodriguez EH, Schaner ME, Salim A, Wang Y, Kristensen GB, Helland A, Borresen-Dale AL, Giaccia A, Longaker MT, Hastie T, Yang GP, Vijver MJ, Brown PO. Gene expression programs in response to hypoxia: cell type specificity and prognostic significance in human cancers. PLoS Med 2006, 3:e47. 10.1371/journal.pmed.0030047, 1334226,1334226, 16417408.
18. Vengellur A, Phillips JM, Hogenesch JB, LaPres JJ. Gene expression profiling of hypoxia signaling in human hepatocellular carcinoma cells. Physiol Genomics 2005, 22:308-318. 10.1152/physiolgenomics.00045.2004, 15942021.
19. Elvidge GP, Glenny L, Appelhoff RJ, Ratcliffe PJ, Ragoussis J, Gleadle JM. Concordant regulation of gene expression by hypoxia and 2-oxoglutarate-dependent dioxygenase inhibition: the role of HIF-1alpha, HIF-2alpha, and other pathways. J Biol Chem 2006, 281:15215-15226. 10.1074/jbc.M511408200, 16565084.
20. Katada K, Naito Y, Mizushima K, Takagi T, Handa O, Kokura S, Ichikawa H, Yoshida N, Matsui H, Yoshikawa T. Gene expression profiles on hypoxia and reoxygenation in rat gastric epithelial cells: a high-density DNA microarray analysis. Digestion 2006, 73:89-100. 10.1159/000094039, 16788290.
21. Sung FL, Hui EP, Tao Q, Li H, Tsui NB, Dennis Lo YM, Ma BB, To KF, Harris AL, Chan AT. Genome-wide expression analysis using microarray identified complex signaling pathways modulated by hypoxia in nasopharyngeal carcinoma. Cancer Lett 2007, 253:74-88. 10.1016/j.canlet.2007.01.012, 17320280.
22. Johnson WE, Li W, Meyer CA, Gottardo R, Carroll JS, Brown M, Liu XS. Model-based analysis of tiling-arrays for ChIP-chip. Proc Natl Acad Sci USA 2006, 103:12457-12462. 10.1073/pnas.0601180103, 1567901, 16895995.
23. Subramanian A, Tamayo P, Mootha VK, Mukherjee S, Ebert BL, Gillette MA, Paulovich A, Pomeroy SL, Golub TR, Lander ES, Mesirov JP. Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. Proc Natl Acad Sci USA 2005, 102:15545-15550. 10.1073/pnas.0506580102, 1239896,1239896, 16199517.
24. Bernstein BE, Kamal M, Lindblad-Toh K, Bekiranov S, Bailey DK, Huebert DJ, McMahon S, Karlsson EK, Kulbokas EJ, Gingeras TR, Schreiber SL, Lander ES. Genomic maps and comparative analysis of histone modifications in human and mouse. Cell 2005, 120:169-181. 10.1016/j.cell.2005.01.001, 15680324.
25. Kim TH, Barrera LO, Zheng M, Qu C, Singer MA, Richmond TA, Wu Y, Green RD, Ren B. A high-resolution map of active promoters in the human genome. Nature 2005, 436:876-880. 10.1038/nature03877, 1895599, 15988478.
26. Barski A, Cuddapah S, Cui K, Roh TY, Schones DE, Wang Z, Wei G, Chepelev I, Zhao K. High-resolution profiling of histone methylations in the human genome. Cell 2007, 129:823-837. 10.1016/j.cell.2007.05.009, 17512414.
27. Yuan GC, Liu YJ, Dion MF, Slack MD, Wu LF, Altschuler SJ, Rando OJ. Genome-scale identification of nucleosome positions in S. cerevisiae. Science 2005, 309:626-630. 10.1126/science.1112178, 15961632.
28. Ozsolak F, Song JS, Liu XS, Fisher DE. High-throughput mapping of the chromatin structure of human promoters. Nat Biotechnol 2007, 25:244-248. 10.1038/nbt1279, 17220878.
29. Guenther MG, Levine SS, Boyer LA, Jaenisch R, Young RA. A chromatin landmark and transcription initiation at most promoters in human cells. Cell 2007, 130:77-88. 10.1016/j.cell.2007.05.042, 17632057.
30. Guccione E, Martinato F, Finocchiaro G, Luzi L, Tizzoni L, Dall' Olio V, Zardo G, Nervi C, Bernard L, Amati B. Myc-binding-site recognition in the human genome is determined by chromatin context. Nat Cell Biol 2006, 8:764-770. 10.1038/ncb1434, 16767079.
31. Kim J, Chu J, Shen X, Wang J, Orkin SH. An extended transcriptional network for pluripotency of embryonic stem cells. Cell 2008, 132:1049-1061. 10.1016/j.cell.2008.02.039, 18358816.
32. Prendergast GC, Lawe D, Ziff EB. Association of Myn, the murine homolog of max, with c-Myc stimulates methylation-sensitive DNA binding and ras cotransformation. Cell 1991, 65:395-407. 10.1016/0092-8674(91)90457-A, 1840505.
33. Cha-Molstad H, Keller DM, Yochum GS, Impey S, Goodman RH. Cell-type-specific binding of the transcription factor CREB to the cAMP-response element. Proc Natl Acad Sci USA 2004, 101:13572-13577. 10.1073/pnas.0405587101, 518796, 15342915.
34. Heintzman ND, Hon GC, Hawkins RD, Kheradpour P, Stark A, Harp LF, Ye Z, Lee LK, Stuart RK, Ching CW, Ching KA, Antosiewicz-Bourget JE, Liu H, Zhang X, Green RD, Lobanenkov VV, Stewart R, Thomson JA, Crawford GE, Kellis M, Ren B. Histone modifications at human enhancers reflect global cell-type-specific gene expression. Nature 2009, 459:108-112. 10.1038/nature07829, 19295514.
35. Dai M, Wang P, Boyd AD, Kostov G, Athey B, Jones EG, Bunney WE, Myers RM, Speed TP, Akil H, Watson SJ, Meng F. Evolving gene/transcript definitions significantly alter the interpretation of GeneChip data. Nucleic Acids Res 2005, 33:e175. 10.1093/nar/gni179, 1283542, 16284200.
36. Gene Set Enrichment Analysis (GSEA) at the Broad Institute. , http://www.broad.mit.edu/gsea/