Home LiteratureArticle Details
PMID: 21924352 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Review

Chromatin as an oxygen sensor and active player in the hypoxia response.

Cellular signalling ·Vol. 24 ·No. 1 ·2012-01-00 ·Pages 35-43

Melvin A, Rocha S

Abstract

Changes in the availability or demand for oxygen induce dramatic changes at the cellular level. Primarily, activation of a family of oxygen labile transcription factors, Hypoxia Inducible Factor (HIF), initiates a variety of cellular processes required to re-instate oxygen homeostasis. Oxygen is sensed by molecular dioxygenases in cells, such as the prolyl-hydroxylases (PHDs), enzymes which are responsible for the oxygen-dependent regulation of HIF. As HIF is a transcription factor it must bind DNA sequences of its target genes possibly in the context of a complex chromatin structure. How chromatin structure changes in response to hypoxia is currently unknown. However, the identification of a novel class of histone demethylases as true dioxygenases suggests that chromatin can act as an oxygen sensor and plays an active role in the coordination of the cellular response to hypoxia. This review will discuss the current knowledge on how hypoxia engages with different proteins involved in chromatin organisation and dynamics.

MeSH Terms
Acetylation Animals Cell Hypoxia Chromatin/metabolism,physiology Chromatin Assembly and Disassembly Gene Expression Regulation Histones/metabolism Humans Hypoxia-Inducible Factor 1/metabolism Methylation Molecular Conformation Oxygen/metabolism Protein Processing, Post-Translational
Chemicals
Chromatin Histones Hypoxia-Inducible Factor 1 Oxygen
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Melvin Andrew
Wellcome Trust Centre for Gene Regulation and Expression, College of Life Sciences, MSI/WTB/JBC Complex, University of Dundee, Dundee, Scotland, United Kingdom.
Rocha Sonia
References (142)
142 references, click to expand
  1. ARNT-deficient mice and placental differentiation.
    Dev Biol. 1997 Nov 15;191(2):297-305 PMID: 9398442
  2. SirT3 suppresses hypoxia inducible factor 1α and tumor growth by inhibiting mitochondrial ROS production.
    Oncogene. 2011 Jun 30;30(26):2986-96 PMID: 21358671
  3. Critical role of HIF-1alpha in keratinocyte defense against bacterial infection.
    J Invest Dermatol. 2008 Aug;128(8):1964-8 PMID: 18323789
  4. Metastasis-associated protein 1 enhances stability of hypoxia-inducible factor-1alpha protein by recruiting histone deacetylase 1.
    EMBO J. 2006 Mar 22;25(6):1231-41 PMID: 16511565
  5. Methylation of the CA9 promoter can modulate expression of the tumor-associated carbonic anhydrase IX in dense carcinoma cell lines.
    Int J Oncol. 2005 Apr;26(4):1121-7 PMID: 15754010
  6. The multifaceted proteins Reptin and Pontin as major players in cancer.
    Biochim Biophys Acta. 2011 Apr;1815(2):147-57 PMID: 21111787
  7. Rsf-1, a chromatin remodeling protein, induces DNA damage and promotes genomic instability.
    J Biol Chem. 2010 Dec 3;285(49):38260-9 PMID: 20923775
  8. Gene regulation under low oxygen: holding your breath for transcription.
    Trends Biochem Sci. 2007 Aug;32(8):389-97 PMID: 17624786
  9. JMJD2A is a novel N-CoR-interacting protein and is involved in repression of the human transcription factor achaete scute-like homologue 2 (ASCL2/Hash2).
    Mol Cell Biol. 2005 Aug;25(15):6404-14 PMID: 16024779
  10. Negative regulation of hypoxic responses via induced Reptin methylation.
    Mol Cell. 2010 Jul 9;39(1):71-85 PMID: 20603076
  11. The conserved role of sirtuins in chromatin regulation.
    Int J Dev Biol. 2009;53(2-3):303-22 PMID: 19378253
  12. The H3K36 demethylase Jhdm1b/Kdm2b regulates cell proliferation and senescence through p15(Ink4b).
    Nat Struct Mol Biol. 2008 Nov;15(11):1169-75 PMID: 18836456
  13. The histone demethylase JMJD2B is regulated by estrogen receptor alpha and hypoxia, and is a key mediator of estrogen induced growth.
    Cancer Res. 2010 Aug 15;70(16):6456-66 PMID: 20682797
  14. Jmjd6 catalyses lysyl-hydroxylation of U2AF65, a protein associated with RNA splicing.
    Science. 2009 Jul 3;325(5936):90-3 PMID: 19574390
  15. SRG3, a core component of mouse SWI/SNF complex, is essential for extra-embryonic vascular development.
    Dev Biol. 2008 Mar 1;315(1):136-46 PMID: 18206867
  16. Hypoxia-induced down-regulation of neprilysin by histone modification in mouse primary cortical and hippocampal neurons.
    PLoS One. 2011 Apr 29;6(4):e19229 PMID: 21559427
  17. Targeted ablation of Arnt in mouse epidermis results in profound defects in desquamation and epidermal barrier function.
    J Cell Sci. 2006 Dec 1;119(Pt 23):4901-12 PMID: 17105764
  18. Abnormal sympathoadrenal development and systemic hypotension in PHD3-/- mice.
    Mol Cell Biol. 2008 May;28(10):3386-400 PMID: 18332118
  19. Obesity and metabolic syndrome in histone demethylase JHDM2a-deficient mice.
    Genes Cells. 2009 Aug;14(8):991-1001 PMID: 19624751
  20. Two transactivation mechanisms cooperate for the bulk of HIF-1-responsive gene expression.
    EMBO J. 2005 Nov 16;24(22):3846-58 PMID: 16237459
  21. JHDM2A, a JmjC-containing H3K9 demethylase, facilitates transcription activation by androgen receptor.
    Cell. 2006 May 5;125(3):483-95 PMID: 16603237
  22. Integrative analysis of HIF binding and transactivation reveals its role in maintaining histone methylation homeostasis.
    Proc Natl Acad Sci U S A. 2009 Mar 17;106(11):4260-5 PMID: 19255431
  23. Effect of hypoxia on hepatic DNA methylation and tRNA methyltransferase in rat: similarities to effects of methyl-deficient diets.
    J Cell Biochem. 1996 Apr;61(1):72-80 PMID: 8726357
  24. The transcription factor EPAS-1/hypoxia-inducible factor 2alpha plays an important role in vascular remodeling.
    Proc Natl Acad Sci U S A. 2000 Jul 18;97(15):8386-91 PMID: 10880563
  25. The chromatin-remodeling enzyme BRG1 plays an essential role in primitive erythropoiesis and vascular development.
    Development. 2008 Feb;135(3):493-500 PMID: 18094026
  26. PHF8, a gene associated with cleft lip/palate and mental retardation, encodes for an Nepsilon-dimethyl lysine demethylase.
    Hum Mol Genet. 2010 Jan 15;19(2):217-22 PMID: 19843542
  27. Histone demethylation mediated by the nuclear amine oxidase homolog LSD1.
    Cell. 2004 Dec 29;119(7):941-53 PMID: 15620353
  28. Multiple organ pathology, metabolic abnormalities and impaired homeostasis of reactive oxygen species in Epas1-/- mice.
    Nat Genet. 2003 Dec;35(4):331-40 PMID: 14608355
  29. A novel gene (PLU-1) containing highly conserved putative DNA/chromatin binding motifs is specifically up-regulated in breast cancer.
    J Biol Chem. 1999 May 28;274(22):15633-45 PMID: 10336460
  30. Role of CBP in regulating HIF-1-mediated activation of transcription.
    J Cell Sci. 2005 Jan 15;118(Pt 2):301-11 PMID: 15615775
  31. Reading, writing and editing methylated lysines on histone tails: new insights from recent structural studies.
    Curr Opin Struct Biol. 2010 Dec;20(6):730-8 PMID: 20956082
  32. Identification and characterization of demethylase JMJD1A as a gene upregulated in the human cellular response to hypoxia.
    Cell Tissue Res. 2009 Aug;337(2):223-34 PMID: 19471969
  33. HIF-1 alpha is required for solid tumor formation and embryonic vascularization.
    EMBO J. 1998 Jun 1;17(11):3005-15 PMID: 9606183
  34. PCAF is an HIF-1alpha cofactor that regulates p53 transcriptional activity in hypoxia.
    Oncogene. 2008 Oct 2;27(44):5785-96 PMID: 18574470
  35. Regulation of adult erythropoiesis by prolyl hydroxylase domain proteins.
    Blood. 2008 Mar 15;111(6):3229-35 PMID: 18056838
  36. Aberrant DNA methylation associated with silencing BNIP3 gene expression in haematopoietic tumours.
    Br J Cancer. 2005 Mar 28;92(6):1165-72 PMID: 15756280
  37. CpG islands and the regulation of transcription.
    Genes Dev. 2011 May 15;25(10):1010-22 PMID: 21576262
  38. Targeting tumor angiogenesis with histone deacetylase inhibitors.
    Cancer Lett. 2009 Aug 8;280(2):145-53 PMID: 19111391
  39. A functional link between the histone demethylase PHF8 and the transcription factor ZNF711 in X-linked mental retardation.
    Mol Cell. 2010 Apr 23;38(2):165-78 PMID: 20346720
  40. The roles of human sucrose nonfermenting protein 2 homologue in the tumor-promoting functions of Rsf-1.
    Cancer Res. 2008 Jun 1;68(11):4050-7 PMID: 18519663
  41. Methylation of histone H3 lysine 36 enhances DNA repair by nonhomologous end-joining.
    Proc Natl Acad Sci U S A. 2011 Jan 11;108(2):540-5 PMID: 21187428
  42. SWI/SNF nucleosome remodellers and cancer.
    Nat Rev Cancer. 2011 Jun 09;11(7):481-92 PMID: 21654818
  43. Jmjd2b antagonizes H3K9 trimethylation at pericentric heterochromatin in mammalian cells.
    Genes Dev. 2006 Jun 15;20(12):1557-62 PMID: 16738407
  44. Regulation of chromatin by histone modifications.
    Cell Res. 2011 Mar;21(3):381-95 PMID: 21321607
  45. Loss of ARNT/HIF1beta mediates altered gene expression and pancreatic-islet dysfunction in human type 2 diabetes.
    Cell. 2005 Aug 12;122(3):337-49 PMID: 16096055
  46. Loss of prolyl hydroxylase-1 protects against colitis through reduced epithelial cell apoptosis and increased barrier function.
    Gastroenterology. 2010 Dec;139(6):2093-101 PMID: 20600011
  47. Epigenetic regulation of surfactant protein A gene (SP-A) expression in fetal lung reveals a critical role for Suv39h methyltransferases during development and hypoxia.
    Mol Cell Biol. 2011 May;31(10):1949-58 PMID: 21402781
  48. Roles of jumonji and jumonji family genes in chromatin regulation and development.
    Dev Dyn. 2006 Sep;235(9):2449-59 PMID: 16715513
  49. Chromatin remodeling factor CHD5 is silenced by promoter CpG island hypermethylation in human cancer.
    Epigenetics. 2008 Jul-Aug;3(4):210-5 PMID: 18698156
  50. Hepatocyte-specific hypoxia-inducible factor-1α is a determinant of lipid accumulation and liver injury in alcohol-induced steatosis in mice.
    Hepatology. 2011 May;53(5):1526-37 PMID: 21520168
  51. Regulation of gene expression by hypoxia.
    Biochem J. 2008 Aug 15;414(1):19-29 PMID: 18651837
  52. The histone demethylases JMJD1A and JMJD2B are transcriptional targets of hypoxia-inducible factor HIF.
    J Biol Chem. 2008 Dec 26;283(52):36542-52 PMID: 18984585
  53. Nucleosome-interacting proteins regulated by DNA and histone methylation.
    Cell. 2010 Oct 29;143(3):470-84 PMID: 21029866
  54. A Brg1 null mutation in the mouse reveals functional differences among mammalian SWI/SNF complexes.
    Mol Cell. 2000 Dec;6(6):1287-95 PMID: 11163203
  55. Role of Jhdm2a in regulating metabolic gene expression and obesity resistance.
    Nature. 2009 Apr 9;458(7239):757-61 PMID: 19194461
  56. Cellular and developmental control of O2 homeostasis by hypoxia-inducible factor 1 alpha.
    Genes Dev. 1998 Jan 15;12(2):149-62 PMID: 9436976
  57. Hypoxia induces trimethylated H3 lysine 4 by inhibition of JARID1A demethylase.
    Cancer Res. 2010 May 15;70(10):4214-21 PMID: 20406991
  58. Chromatin higher-order structures and gene regulation.
    Curr Opin Genet Dev. 2011 Apr;21(2):175-86 PMID: 21342762
  59. Histone variants in metazoan development.
    Dev Cell. 2010 Nov 16;19(5):662-74 PMID: 21074717
  60. Hypoxia induces a novel signature of chromatin modifications and global repression of transcription.
    Mutat Res. 2008 Apr 2;640(1-2):174-9 PMID: 18294659
  61. The SirT3 divining rod points to oxidative stress.
    Mol Cell. 2011 Jun 10;42(5):561-8 PMID: 21658599
  62. The putative oncogene GASC1 demethylates tri- and dimethylated lysine 9 on histone H3.
    Nature. 2006 Jul 20;442(7100):307-11 PMID: 16732293
  63. Multiple facets of the unique histone variant macroH2A: from genomics to cell biology.
    Cell Cycle. 2010 Jul 1;9(13):2568-74 PMID: 20543561
  64. Placental but not heart defects are associated with elevated hypoxia-inducible factor alpha levels in mice lacking prolyl hydroxylase domain protein 2.
    Mol Cell Biol. 2006 Nov;26(22):8336-46 PMID: 16966370
  65. Epithelial hypoxia-inducible factor-1 is protective in murine experimental colitis.
    J Clin Invest. 2004 Oct;114(8):1098-106 PMID: 15489957
  66. Altered control of cellular proliferation in the absence of mammalian brahma (SNF2alpha).
    EMBO J. 1998 Dec 1;17(23):6979-91 PMID: 9843504
  67. The ISWI ATPase Snf2h is required for early mouse development.
    Proc Natl Acad Sci U S A. 2003 Nov 25;100(24):14097-102 PMID: 14617767
  68. Loss or silencing of the PHD1 prolyl hydroxylase protects livers of mice against ischemia/reperfusion injury.
    Gastroenterology. 2010 Mar;138(3):1143-54.e1-2 PMID: 19818783
  69. Hypoxia causes epigenetic gene regulation in macrophages by attenuating Jumonji histone demethylase activity.
    Cytokine. 2011 Feb;53(2):256-62 PMID: 21131212
  70. Targeting hypoxic cells through the DNA damage response.
    Clin Cancer Res. 2010 Dec 1;16(23):5624-9 PMID: 20876254
  71. Roles of Brahma and Brahma/SWI2-related gene 1 in hypoxic induction of the erythropoietin gene.
    J Biol Chem. 2004 Nov 5;279(45):46733-41 PMID: 15347669
  72. PKA-dependent regulation of the histone lysine demethylase complex PHF2-ARID5B.
    Nat Cell Biol. 2011 Jun;13(6):668-75 PMID: 21532585
  73. Genome-wide association of hypoxia-inducible factor (HIF)-1alpha and HIF-2alpha DNA binding with expression profiling of hypoxia-inducible transcripts.
    J Biol Chem. 2009 Jun 19;284(25):16767-16775 PMID: 19386601
  74. Ischemia dysregulates DNA methyltransferases and p16INK4a methylation in human colorectal cancer cells.
    Epigenetics. 2010 Aug 16;5(6):547-56 PMID: 20543577
  75. Structure and mechanisms of lysine methylation recognition by the chromodomain in gene transcription.
    Biochemistry. 2011 Mar 29;50(12):1966-80 PMID: 21288002
  76. DNA methylation analysis of the HIF-1α prolyl hydroxylase domain genes PHD1, PHD2, PHD3 and the factor inhibiting HIF gene FIH in invasive breast carcinomas.
    Histopathology. 2010 Sep;57(3):451-60 PMID: 20727020
  77. Structure and function of histone H3 lysine 9 methyltransferases and demethylases.
    Chembiochem. 2011 Jan 24;12(2):254-63 PMID: 21243713
  78. Loss of HIF-2alpha and inhibition of VEGF impair fetal lung maturation, whereas treatment with VEGF prevents fatal respiratory distress in premature mice.
    Nat Med. 2002 Jul;8(7):702-10 PMID: 12053176
  79. Histone variants--ancient wrap artists of the epigenome.
    Nat Rev Mol Cell Biol. 2010 Apr;11(4):264-75 PMID: 20197778
  80. Induction of DNA hypomethylation by tumor hypoxia.
    Epigenetics. 2007 Apr-Jun;2(2):119-25 PMID: 17965619
  81. Developmental roles of the histone lysine demethylases.
    Development. 2009 Mar;136(6):879-89 PMID: 19234061
  82. The Jmjd3-Irf4 axis regulates M2 macrophage polarization and host responses against helminth infection.
    Nat Immunol. 2010 Oct;11(10):936-44 PMID: 20729857
  83. Cooperative demethylation by JMJD2C and LSD1 promotes androgen receptor-dependent gene expression.
    Nat Cell Biol. 2007 Mar;9(3):347-53 PMID: 17277772
  84. The asparaginyl hydroxylase factor inhibiting HIF-1alpha is an essential regulator of metabolism.
    Cell Metab. 2010 May 5;11(5):364-78 PMID: 20399150
  85. The site-specific installation of methyl-lysine analogs into recombinant histones.
    Cell. 2007 Mar 9;128(5):1003-12 PMID: 17350582
  86. Metastasis-associated protein 1 enhances angiogenesis by stabilization of HIF-1alpha.
    Oncol Rep. 2006 Oct;16(4):929-35 PMID: 16969516
  87. Regulation of the histone demethylase JMJD1A by hypoxia-inducible factor 1 alpha enhances hypoxic gene expression and tumor growth.
    Mol Cell Biol. 2010 Jan;30(1):344-53 PMID: 19858293
  88. Disruption of Trrap causes early embryonic lethality and defects in cell cycle progression.
    Nat Genet. 2001 Oct;29(2):206-11 PMID: 11544477
  89. JmjC enzyme KDM2A is a regulator of rRNA transcription in response to starvation.
    EMBO J. 2010 May 5;29(9):1510-22 PMID: 20379134
  90. Identification of a novel gene, GASC1, within an amplicon at 9p23-24 frequently detected in esophageal cancer cell lines.
    Cancer Res. 2000 Sep 1;60(17):4735-9 PMID: 10987278
  91. Tumor suppressor gene identification using retroviral insertional mutagenesis in Blm-deficient mice.
    EMBO J. 2006 Jul 26;25(14):3422-31 PMID: 16858412
  92. Physiological and biochemical aspects of hydroxylations and demethylations catalyzed by human 2-oxoglutarate oxygenases.
    Trends Biochem Sci. 2011 Jan;36(1):7-18 PMID: 20728359
  93. The human side of hypoxia-inducible factor.
    Br J Haematol. 2008 May;141(3):325-34 PMID: 18410568
  94. Adenomatous polyposis coli and hypoxia-inducible factor-1{alpha} have an antagonistic connection.
    Mol Biol Cell. 2010 Nov 1;21(21):3630-8 PMID: 20844082
  95. Chromatin remodelling during development.
    Nature. 2010 Jan 28;463(7280):474-84 PMID: 20110991
  96. Deficiency or inhibition of oxygen sensor Phd1 induces hypoxia tolerance by reprogramming basal metabolism.
    Nat Genet. 2008 Feb;40(2):170-80 PMID: 18176562
  97. Essential role for prolyl hydroxylase domain protein 2 in oxygen homeostasis of the adult vascular system.
    Circulation. 2007 Aug 14;116(7):774-81 PMID: 17646578
  98. SIRT3 controls cancer metabolic reprogramming by regulating ROS and HIF.
    Cancer Cell. 2011 Mar 8;19(3):299-300 PMID: 21397853
  99. Lack of hypoxia-inducible factor-1 alpha impairs midbrain neural precursor cells involving vascular endothelial growth factor signaling.
    J Neurosci. 2007 Jan 10;27(2):412-21 PMID: 17215402
  100. HIF-1alpha is essential for myeloid cell-mediated inflammation.
    Cell. 2003 Mar 7;112(5):645-57 PMID: 12628185
  101. Hypoxic stress induces dimethylated histone H3 lysine 9 through histone methyltransferase G9a in mammalian cells.
    Cancer Res. 2006 Sep 15;66(18):9009-16 PMID: 16982742
  102. Hypoxia induces genomic DNA demethylation through the activation of HIF-1α and transcriptional upregulation of MAT2A in hepatoma cells.
    Mol Cancer Ther. 2011 Jun;10(6):1113-23 PMID: 21460102
  103. PLU-1 nuclear protein, which is upregulated in breast cancer, shows restricted expression in normal human adult tissues: a new cancer/testis antigen?
    Int J Cancer. 2002 Oct 20;101(6):581-8 PMID: 12237901
  104. Hypoxia increases sirtuin 1 expression in a hypoxia-inducible factor-dependent manner.
    J Biol Chem. 2011 Apr 22;286(16):13869-78 PMID: 21345792
  105. T cell-specific disruption of arylhydrocarbon receptor nuclear translocator (Arnt) gene causes resistance to 2,3,7,8-tetrachlorodibenzo-p-dioxin-induced thymic involution.
    J Immunol. 2003 Oct 15;171(8):4113-20 PMID: 14530333
  106. PLU-1 is an H3K4 demethylase involved in transcriptional repression and breast cancer cell proliferation.
    Mol Cell. 2007 Mar 23;25(6):801-12 PMID: 17363312
  107. High-resolution genome-wide mapping of HIF-binding sites by ChIP-seq.
    Blood. 2011 Jun 9;117(23):e207-17 PMID: 21447827
  108. CpG islands recruit a histone H3 lysine 36 demethylase.
    Mol Cell. 2010 Apr 23;38(2):179-90 PMID: 20417597
  109. Identification of multiple distinct Snf2 subfamilies with conserved structural motifs.
    Nucleic Acids Res. 2006 May 31;34(10):2887-905 PMID: 16738128
  110. Increased protein arginine methylation in chronic hypoxia: role of protein arginine methyltransferases.
    Am J Respir Cell Mol Biol. 2006 Oct;35(4):436-43 PMID: 16690984
  111. Independent function of two destruction domains in hypoxia-inducible factor-alpha chains activated by prolyl hydroxylation.
    EMBO J. 2001 Sep 17;20(18):5197-206 PMID: 11566883
  112. Chromatin remodelling in mammalian cells by ISWI-type complexes--where, when and why?
    FEBS J. 2011 Oct;278(19):3608-18 PMID: 21810179
  113. Regulation of hypoxia-inducible factor 2alpha signaling by the stress-responsive deacetylase sirtuin 1.
    Science. 2009 Jun 5;324(5932):1289-93 PMID: 19498162
  114. Chromatin remodelling beyond transcription: the INO80 and SWR1 complexes.
    Nat Rev Mol Cell Biol. 2009 Jun;10(6):373-84 PMID: 19424290
  115. Structure and acetyl-lysine recognition of the bromodomain.
    Oncogene. 2007 Aug 13;26(37):5521-7 PMID: 17694091
  116. Transcriptome remodeling in hypoxic inflammation.
    J Dent Res. 2010 May;89(5):430-44 PMID: 20348484
  117. Role of hypoxia-inducible factors in epigenetic regulation via histone demethylases.
    Ann N Y Acad Sci. 2009 Oct;1177:185-97 PMID: 19845621
  118. Placental defects in ARNT-knockout conceptus correlate with localized decreases in VEGF-R2, Ang-1, and Tie-2.
    Dev Dyn. 2000 Dec;219(4):526-38 PMID: 11084652
  119. Systematic protein location mapping reveals five principal chromatin types in Drosophila cells.
    Cell. 2010 Oct 15;143(2):212-24 PMID: 20888037
  120. DNA methylation and demethylation in mammals.
    J Biol Chem. 2011 May 27;286(21):18347-53 PMID: 21454628
  121. ATP-dependent chromatin remodeling: genetics, genomics and mechanisms.
    Cell Res. 2011 Mar;21(3):396-420 PMID: 21358755
  122. Regulation of Jumonji-domain-containing histone demethylases by hypoxia-inducible factor (HIF)-1alpha.
    Biochem J. 2008 Dec 15;416(3):387-94 PMID: 18713068
  123. Hypoxia-induced methylation of a pontin chromatin remodeling factor.
    Proc Natl Acad Sci U S A. 2011 Aug 16;108(33):13510-5 PMID: 21825155
  124. Mechanisms for ATP-dependent chromatin remodelling: the means to the end.
    FEBS J. 2011 Oct;278(19):3579-95 PMID: 21810178
  125. Hairless is a nuclear receptor corepressor essential for skin function.
    Nucl Recept Signal. 2009 Dec 31;7:e010 PMID: 20087431
  126. Histone demethylase JMJD2B coordinates H3K4/H3K9 methylation and promotes hormonally responsive breast carcinogenesis.
    Proc Natl Acad Sci U S A. 2011 May 3;108(18):7541-6 PMID: 21502505
  127. Defective vascularization of HIF-1alpha-null embryos is not associated with VEGF deficiency but with mesenchymal cell death.
    Dev Biol. 1999 May 15;209(2):254-67 PMID: 10328919
  128. Sirtuin 1 modulates cellular responses to hypoxia by deacetylating hypoxia-inducible factor 1alpha.
    Mol Cell. 2010 Jun 25;38(6):864-78 PMID: 20620956
  129. Histone H2AX is integral to hypoxia-driven neovascularization.
    Nat Med. 2009 May;15(5):553-8 PMID: 19377486
  130. Defective brain development in mice lacking the Hif-1alpha gene in neural cells.
    Mol Cell Biol. 2003 Oct;23(19):6739-49 PMID: 12972594
  131. The histone deacetylase Sirt6 regulates glucose homeostasis via Hif1alpha.
    Cell. 2010 Jan 22;140(2):280-93 PMID: 20141841
  132. Genetic and expressional alterations of CHD genes in gastric and colorectal cancers.
    Histopathology. 2011 Apr;58(5):660-8 PMID: 21447119
  133. Systematic sequencing of renal carcinoma reveals inactivation of histone modifying genes.
    Nature. 2010 Jan 21;463(7279):360-3 PMID: 20054297
  134. Silencing of the hypoxia-inducible cell death protein BNIP3 in pancreatic cancer.
    Cancer Res. 2004 Aug 1;64(15):5338-46 PMID: 15289340
  135. Aberrant promoter CpG methylation is a mechanism for impaired PHD3 expression in a diverse set of malignant cells.
    PLoS One. 2011 Jan 28;6(1):e14617 PMID: 21297970
  136. SWI/SNF: the crossroads where extracellular signaling pathways meet chromatin.
    J Cell Physiol. 2006 May;207(2):309-14 PMID: 16155938
  137. SWI/SNF regulates the cellular response to hypoxia.
    J Biol Chem. 2009 Feb 13;284(7):4123-31 PMID: 19097995
  138. Composition and functional specificity of SWI2/SNF2 class chromatin remodeling complexes.
    Biochim Biophys Acta. 2005 Jan 11;1681(2-3):59-73 PMID: 15627498
  139. Roles of coactivators in hypoxic induction of the erythropoietin gene.
    PLoS One. 2010 Apr 02;5(4):e10002 PMID: 20368990
  140. Exome sequencing identifies frequent mutation of the SWI/SNF complex gene PBRM1 in renal carcinoma.
    Nature. 2011 Jan 27;469(7331):539-42 PMID: 21248752
  141. Hypoxia and nickel inhibit histone demethylase JMJD1A and repress Spry2 expression in human bronchial epithelial BEAS-2B cells.
    Carcinogenesis. 2010 Dec;31(12):2136-44 PMID: 20881000
  142. Hypoxia upregulates the histone demethylase JMJD1A via HIF-1.
    Biochem Biophys Res Commun. 2008 Aug 8;372(4):892-7 PMID: 18538129
Article Info
Journal
Cellular signalling
Abbr.
Cell Signal
ISSN
1873-3913
DOI
10.1016/j.cellsig.2011.08.019
Published
2012-01-00
Epub
2011-00-08
Pages
35-43
Language
English
Region
England
NLM ID
8904683
PMCID
PMC3476533
Subset
IM
Grants
Wellcome Trust · 083524 · United Kingdom
Cancer Research UK · 12918 · United Kingdom
Cancer Research UK · A12918 · United Kingdom
External Links
PubMed source DOI: 10.1016/j.cellsig.2011.08.019 PMC Full Text View journal details
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com

Copyright © 2026.Genelibs Jinan Honghui Biotechnology Co., Ltd. 鲁ICP备20007159号-2