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PMID: 15242350 Published · ppublish English Journal Article Research Support, U.S. Gov't, P.H.S.

Upstream stimulatory factors, USF1 and USF2, bind to the human haem oxygenase-1 proximal promoter in vivo and regulate its transcription.

The Biochemical journal ·Vol. 383 ·No. Pt 2 ·2004-10-15 ·Pages 209-18

Hock TD, Nick HS, Agarwal A

Abstract

The human HO-1 (haem oxygenase-1) gene encodes a microsomal enzyme responsible for the breakdown of haem, and is also cytoprotective in response to various cellular insults. HO-1 transcription is induced by a vast array of compounds including, but certainly not limited to, haem and heavy metals such as cadmium. In the present study, we show that upstream stimulatory factors, USF1 and USF2, ubiquitous proteins belonging to the basic helix-loop-helix-leucine zipper family of transcription factors, constitutively bind to the class B E-box located in the proximal promoter of the human HO-1 gene and are responsible for the enhancement of HO-1 gene transcription in human renal proximal tubular epithelial cells. Dimethylsulphate in vivo footprinting studies have identified three protected guanine residues in the E-box of the HO-1 proximal promoter. One of these guanine contact points is essential for USF binding, and when mutated mimics a deletion mutation of the entire E-box palindrome sequence encompassing all three guanine contact points. Binding of USF1 and USF2 to the HO-1 E-box was confirmed by chromatin immunoprecipitation and gel-shift assays. Furthermore, we show that overexpression of USF1 or USF2 enhances the basal expression of HO-1 and that expression of a USF dominant negative form reduces its expression. These results demonstrate for the first time that USF proteins bind to the human HO-1 promoter in vivo and are required for high-level expression of HO-1 by haem and cadmium in human renal epithelial cells.

MeSH Terms
Animals Base Sequence Binding Sites Cadmium/pharmacology Cell Line Chromatin Immunoprecipitation DNA/genetics,metabolism DNA Footprinting DNA-Binding Proteins/genetics,metabolism Electrophoretic Mobility Shift Assay Epithelial Cells Gene Expression Regulation Genes, Dominant/genetics Guanine/metabolism Heme/pharmacology Heme Oxygenase (Decyclizing)/genetics Heme Oxygenase-1 Humans Kidney Membrane Proteins Promoter Regions, Genetic/genetics Protein Binding RNA, Messenger/genetics,metabolism Response Elements/genetics Sulfuric Acid Esters/pharmacology Transcription Factors/genetics,metabolism Transcription, Genetic/genetics Upstream Stimulatory Factors
Chemicals
DNA-Binding Proteins Membrane Proteins RNA, Messenger Sulfuric Acid Esters Transcription Factors USF1 protein, human USF2 protein, human Upstream Stimulatory Factors Cadmium Heme Guanine DNA HMOX1 protein, human Heme Oxygenase (Decyclizing) Heme Oxygenase-1 dimethyl sulfate
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Hock Thomas D
Division of Nephrology, Department of Medicine, University of Alabama at Birmingham, 1530 3rd Avenue South, Birmingham, AL 35294, USA.
Nick Harry S
Agarwal Anupam
References (55)
55 references, click to expand
  1. Combining chromatin immunoprecipitation and DNA footprinting: a novel method to analyze protein-DNA interactions in vivo.
    Nucleic Acids Res. 2002 May 15;30(10):e44 PMID: 12000849
  2. Upstream stimulatory factor regulates major histocompatibility complex class I gene expression: the U2DeltaE4 splice variant abrogates E-box activity.
    Mol Cell Biol. 1999 Jul;19(7):4788-97 PMID: 10373528
  3. USF-1 and USF-2 trans-repress IL-1beta-induced iNOS transcription in mesangial cells.
    Am J Physiol Cell Physiol. 2002 Oct;283(4):C1065-72 PMID: 12225970
  4. Characterization of the human beta-globin downstream promoter region.
    Nucleic Acids Res. 2003 Feb 15;31(4):1292-301 PMID: 12582249
  5. Regulation of human beta 2-microglobulin transactivation in hematopoietic cells.
    Blood. 2003 Apr 15;101(8):3058-64 PMID: 12480693
  6. Upstream stimulatory factors are mediators of Ca2+-responsive transcription in neurons.
    J Neurosci. 2003 Apr 1;23(7):2572-81 PMID: 12684442
  7. Repression of heme oxygenase-1 expression as a defense strategy in humans.
    Exp Biol Med (Maywood). 2003 May;228(5):472-3 PMID: 12709571
  8. An internal enhancer regulates heme- and cadmium-mediated induction of human heme oxygenase-1.
    Am J Physiol Renal Physiol. 2003 Sep;285(3):F515-23 PMID: 12783778
  9. The IGF2 receptor is a USF2-specific target in nontumorigenic mammary epithelial cells but not in breast cancer cells.
    J Biol Chem. 2003 Sep 26;278(39):37231-40 PMID: 12857727
  10. Upstream stimulatory factor but not c-Myc enhances transcription of the human polymeric immunoglobulin receptor gene.
    Mol Immunol. 2004 Jan;40(10):695-708 PMID: 14644095
  11. Transcription of cathepsin B in glioma cells: regulation by an E-box adjacent to the transcription initiation site.
    Biol Chem. 2003 Oct-Nov;384(10-11):1421-7 PMID: 14669984
  12. Transcriptional regulation of human excitatory amino acid transporter 1 (EAAT1): cloning of the EAAT1 promoter and characterization of its basal and inducible activity in human astrocytes.
    J Neurochem. 2003 Dec;87(6):1485-98 PMID: 14713304
  13. The story so far: Molecular regulation of the heme oxygenase-1 gene in renal injury.
    Am J Physiol Renal Physiol. 2004 Mar;286(3):F425-41 PMID: 14761930
  14. Interaction of a gene-specific transcription factor with the adenovirus major late promoter upstream of the TATA box region.
    Cell. 1985 Nov;43(1):165-75 PMID: 4075392
  15. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction.
    Anal Biochem. 1987 Apr;162(1):156-9 PMID: 2440339
  16. The bidirectional upstream element of the adenovirus-2 major late promoter binds a single monomeric molecule of the upstream factor.
    EMBO J. 1987 Oct;6(10):3027-34 PMID: 2826128
  17. Structural organization of the human heme oxygenase gene and the function of its promoter.
    Eur J Biochem. 1989 Feb 15;179(3):557-63 PMID: 2537723
  18. A yeast protein possesses the DNA-binding properties of the adenovirus major late transcription factor.
    Mol Cell Biol. 1989 Feb;9(2):820-2 PMID: 2651905
  19. Transcriptional control of the rat heme oxygenase gene by a nuclear protein that interacts with adenovirus 2 major late promoter.
    J Biol Chem. 1989 Jun 15;264(17):10251-60 PMID: 2722866
  20. Interaction of upstream stimulatory factor with the human heme oxygenase gene promoter.
    Eur J Biochem. 1990 Mar 10;188(2):231-7 PMID: 2318208
  21. Members of the USF family of helix-loop-helix proteins bind DNA as homo- as well as heterodimers.
    Gene Expr. 1992;2(3):231-40 PMID: 1450663
  22. Ultraviolet A (320-380 nm) radiation causes an alteration in the binding of a specific protein/protein complex to a short region of the promoter of the human heme oxygenase 1 gene.
    Nucleic Acids Res. 1993 Mar 11;21(5):1103-9 PMID: 7840819
  23. Interactions of coiled coils in transcription factors: where is the specificity?
    Curr Opin Genet Dev. 1993 Apr;3(2):278-85 PMID: 8504253
  24. In vivo footprinting and genomic sequencing by ligation-mediated PCR.
    Anal Biochem. 1993 Sep;213(2):179-93 PMID: 8238889
  25. HK-2: an immortalized proximal tubule epithelial cell line from normal adult human kidney.
    Kidney Int. 1994 Jan;45(1):48-57 PMID: 8127021
  26. Ubiquitous expression of the 43- and 44-kDa forms of transcription factor USF in mammalian cells.
    Nucleic Acids Res. 1994 Feb 11;22(3):427-33 PMID: 8127680
  27. Identification of binding sites for transcription factors NF-kappa B and AP-2 in the promoter region of the human heme oxygenase 1 gene.
    Proc Natl Acad Sci U S A. 1994 Jun 21;91(13):5987-91 PMID: 8016102
  28. Identification of a cis-acting element that is responsible for cadmium-mediated induction of the human heme oxygenase gene.
    J Biol Chem. 1994 Sep 9;269(36):22858-67 PMID: 8077238
  29. Upstream stimulatory factor regulates expression of the cell cycle-dependent cyclin B1 gene promoter.
    Mol Cell Biol. 1995 May;15(5):2782-90 PMID: 7739559
  30. Transfection of the human heme oxygenase gene into rabbit coronary microvessel endothelial cells: protective effect against heme and hemoglobin toxicity.
    Proc Natl Acad Sci U S A. 1995 Jul 18;92(15):6798-802 PMID: 7624322
  31. Induction of heme oxygenase in toxic renal injury: a protective role in cisplatin nephrotoxicity in the rat.
    Kidney Int. 1995 Oct;48(4):1298-307 PMID: 8569092
  32. Immunochemical characterization and transacting properties of upstream stimulatory factor isoforms.
    J Biol Chem. 1996 Jan 19;271(3):1405-15 PMID: 8576131
  33. Antiproliferative properties of the USF family of helix-loop-helix transcription factors.
    Proc Natl Acad Sci U S A. 1996 Feb 6;93(3):1308-13 PMID: 8577760
  34. Participation of altered upstream stimulatory factor in the induction of rat heme oxygenase-1 by cadmium.
    Nucleic Acids Res. 1996 Aug 1;24(15):2959-65 PMID: 8760880
  35. The heme oxygenase system: a regulator of second messenger gases.
    Annu Rev Pharmacol Toxicol. 1997;37:517-54 PMID: 9131263
  36. Isolation and characterization of a cDNA from the rat brain that encodes hemoprotein heme oxygenase-3.
    Eur J Biochem. 1997 Jul 15;247(2):725-32 PMID: 9266719
  37. Reduced stress defense in heme oxygenase 1-deficient cells.
    Proc Natl Acad Sci U S A. 1997 Sep 30;94(20):10925-30 PMID: 9380736
  38. A general method to design dominant negatives to B-HLHZip proteins that abolish DNA binding.
    Proc Natl Acad Sci U S A. 1997 Nov 11;94(23):12274-9 PMID: 9356439
  39. Overlapping roles and asymmetrical cross-regulation of the USF proteins in mice.
    Proc Natl Acad Sci U S A. 1998 Mar 31;95(7):3758-63 PMID: 9520440
  40. Linoleyl hydroperoxide transcriptionally upregulates heme oxygenase-1 gene expression in human renal epithelial and aortic endothelial cells.
    J Am Soc Nephrol. 1998 Nov;9(11):1990-7 PMID: 9808084
  41. Heme oxygenase: protective gene or Trojan horse.
    Nat Med. 1998 Dec;4(12):1364-5 PMID: 9846569
  42. Oxidative stress causes enhanced endothelial cell injury in human heme oxygenase-1 deficiency.
    J Clin Invest. 1999 Jan;103(1):129-35 PMID: 9884342
  43. Cell-type-dependent activity of the ubiquitous transcription factor USF in cellular proliferation and transcriptional activation.
    Mol Cell Biol. 1999 Feb;19(2):1508-17 PMID: 9891084
  44. In vivo architecture of the manganese superoxide dismutase promoter.
    J Biol Chem. 1999 Feb 5;274(6):3345-54 PMID: 9920876
  45. Upregulation of human heme oxygenase gene expression by Ets-family proteins.
    J Cell Biochem. 1999 Mar 1;72(3):311-21 PMID: 10022513
  46. Yeast and human TATA-binding proteins have nearly identical DNA sequence requirements for transcription in vitro.
    Mol Cell Biol. 1990 Aug;10(8):3859-67 PMID: 2196437
  47. Induction of heme oxygenase is a rapid, protective response in rhabdomyolysis in the rat.
    J Clin Invest. 1992 Jul;90(1):267-70 PMID: 1634613
  48. Positive and negative regulation of the human heme oxygenase-1 gene expression in cultured cells.
    Biochim Biophys Acta. 1999 Oct 28;1447(2-3):231-5 PMID: 10542320
  49. Renal response to tissue injury: lessons from heme oxygenase-1 GeneAblation and expression.
    J Am Soc Nephrol. 2000 May;11(5):965-73 PMID: 10770977
  50. The indispensability of heme oxygenase-1 in protecting against acute heme protein-induced toxicity in vivo.
    Am J Pathol. 2000 May;156(5):1527-35 PMID: 10793064
  51. Heme oxygenase-1 gene ablation or expression modulates cisplatin-induced renal tubular apoptosis.
    Am J Physiol Renal Physiol. 2000 May;278(5):F726-36 PMID: 10807584
  52. Activation of the human asparagine synthetase gene by the amino acid response and the endoplasmic reticulum stress response pathways occurs by common genomic elements.
    J Biol Chem. 2000 Sep 1;275(35):26976-85 PMID: 10856289
  53. Induction of the BRCA2 promoter by nuclear factor-kappa B.
    J Biol Chem. 2000 Nov 10;275(45):35548-56 PMID: 10961992
  54. USF/c-Myc enhances, while Yin-Yang 1 suppresses, the promoter activity of CXCR4, a coreceptor for HIV-1 entry.
    J Immunol. 1999 May 15;162(10):5986-92 PMID: 10229837
  55. ChREBP rather than USF2 regulates glucose stimulation of endogenous L-pyruvate kinase expression in insulin-secreting cells.
    J Biol Chem. 2002 Sep 6;277(36):32746-52 PMID: 12087089
Article Info
Journal
The Biochemical journal
Abbr.
Biochem J
ISSN
1470-8728
Published
2004-10-15
Pages
209-18
Language
English
Region
England
NLM ID
2984726R
PMCID
PMC1134061
Subset
IM
Grants
NIDDK NIH HHS · R01 DK059600 · United States
NHLBI NIH HHS · R01 HL068157 · United States
NIDDK NIH HHS · R01 DK59600 · United States
NHLBI NIH HHS · R01 HL68157 · United States
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