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PMID: 14699086 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Stress-induced transcription of satellite III repeats.

The Journal of cell biology ·Vol. 164 ·No. 1 ·2004-01-05 ·Pages 25-33

Jolly C, Metz A, Govin J, Vigneron M, Turner BM, Khochbin S, Vourc'h C

Abstract

Exposure of mammalian cells to stress induces the activation of heat shock transcription factor 1 (HSF1) and the subsequent transcription of heat shock genes. Activation of the heat shock response also correlates with a rapid relocalization of HSF1 within a few nuclear structures termed nuclear stress granules. These stress-induced structures, which form primarily on the 9q12 region in humans through direct binding of HSF1 to satellite III repeats, do not colocalize with transcription sites of known hsp genes. In this paper, we show that nuclear stress granules correspond to RNA polymerase II transcription factories where satellite III repeats are transcribed into large and stable RNAs that remain associated with the 9q12 region, even throughout mitosis. This work not only reveals the existence of a new major heat-induced transcript in human cells that may play a role in chromatin structure, but also provides evidence for a transcriptional activity within a locus considered so far as heterochromatic and silent.

MeSH Terms
Acetylation CREB-Binding Protein Cell Nucleus Structures/genetics,metabolism,ultrastructure Chromosomes, Human, Pair 9/genetics DNA, Satellite/genetics DNA-Binding Proteins/genetics,metabolism HeLa Cells Heat Shock Transcription Factors Heterochromatin/genetics Histones/genetics,metabolism Humans Nuclear Proteins/genetics,metabolism Protein Transport/genetics RNA/biosynthesis,genetics RNA Polymerase II/biosynthesis Stress, Physiological/genetics,metabolism Trans-Activators/genetics,metabolism Transcription Factors Transcriptional Activation/genetics
Chemicals
DNA, Satellite DNA-Binding Proteins HSF1 protein, human Heat Shock Transcription Factors Heterochromatin Histones Nuclear Proteins Trans-Activators Transcription Factors RNA CREB-Binding Protein CREBBP protein, human RNA Polymerase II
Authors & Affiliations
7 authors, click to expand affiliations / ORCID
Jolly Caroline
INSERM U309, Institut A. Bonniot, 38706 La Tronche cedex, France. caroline.jolly@ujf-grenoble.fr
Metz Alexandra
Govin Jérôme
Vigneron Marc
Turner Bryan M
Khochbin Saadi
Vourc'h Claire
References (50)
50 references, click to expand
  1. Various rat adult tissues express only one major mRNA species from the glyceraldehyde-3-phosphate-dehydrogenase multigenic family.
    Nucleic Acids Res. 1985 Mar 11;13(5):1431-42 PMID: 2987824
  2. Silk worm Bm1 SINE RNA increases following cellular insults.
    Nucleic Acids Res. 1999 Aug 15;27(16):3380-7 PMID: 10454647
  3. Specific antibodies reveal ordered and cell-cycle-related use of histone-H4 acetylation sites in mammalian cells.
    Eur J Biochem. 1989 Jan 15;179(1):131-9 PMID: 2917555
  4. A human chromosome 9-specific alphoid DNA repeat spatially resolvable from satellite 3 DNA by fluorescent in situ hybridization.
    Genomics. 1991 Mar;9(3):517-23 PMID: 1840567
  5. Highly conserved repetitive DNA sequences are present at human centromeres.
    Proc Natl Acad Sci U S A. 1992 Mar 1;89(5):1695-9 PMID: 1542662
  6. Activation of heat shock gene transcription by heat shock factor 1 involves oligomerization, acquisition of DNA-binding activity, and nuclear localization and can occur in the absence of stress.
    Mol Cell Biol. 1993 Mar;13(3):1392-407 PMID: 8441385
  7. Synthesis and maturation of viral transcripts in herpes simplex virus type 1 infected HeLa cells: the role of interchromatin granules.
    Gene Expr. 1995;4(3):143-61 PMID: 7734948
  8. Transcripts from opposite strands of gamma satellite DNA are differentially expressed during mouse development.
    Mamm Genome. 1995 Feb;6(2):76-83 PMID: 7767009
  9. Accurate transcription initiation by RNA polymerase II in a soluble extract from isolated mammalian nuclei.
    Nucleic Acids Res. 1983 Mar 11;11(5):1475-89 PMID: 6828386
  10. Structure and expression of the human gene encoding major heat shock protein HSP70.
    Mol Cell Biol. 1985 Feb;5(2):330-41 PMID: 2858050
  11. The histone acetyltransferase, hGCN5, interacts with and acetylates the HIV transactivator, Tat.
    J Biol Chem. 2001 Jul 27;276(30):28179-84 PMID: 11384967
  12. Stress induction of Bm1 RNA in silkworm larvae: SINEs, an unusual class of stress genes.
    Cell Stress Chaperones. 2001 Jul;6(3):263-72 PMID: 11599568
  13. Stress-induced nuclear bodies are sites of accumulation of pre-mRNA processing factors.
    Mol Biol Cell. 2001 Nov;12(11):3502-14 PMID: 11694584
  14. In vivo binding of active heat shock transcription factor 1 to human chromosome 9 heterochromatin during stress.
    J Cell Biol. 2002 Mar 4;156(5):775-81 PMID: 11877455
  15. X-chromosome inactivation and the search for chromosome-wide silencers.
    Curr Opin Genet Dev. 2002 Apr;12(2):219-24 PMID: 11893496
  16. Higher-order structure in pericentric heterochromatin involves a distinct pattern of histone modification and an RNA component.
    Nat Genet. 2002 Mar;30(3):329-34 PMID: 11850619
  17. Tip60 is targeted to proteasome-mediated degradation by Mdm2 and accumulates after UV irradiation.
    EMBO J. 2002 Apr 2;21(7):1704-12 PMID: 11927554
  18. Human chromosomes 9, 12, and 15 contain the nucleation sites of stress-induced nuclear bodies.
    Mol Biol Cell. 2002 Jun;13(6):2069-79 PMID: 12058070
  19. Small RNAs correspond to centromere heterochromatic repeats.
    Science. 2002 Sep 13;297(5588):1831 PMID: 12193644
  20. Molecular biology. An RNA-guided pathway for the epigenome.
    Science. 2002 Sep 27;297(5590):2215-8 PMID: 12351775
  21. Cellular memory and the histone code.
    Cell. 2002 Nov 1;111(3):285-91 PMID: 12419240
  22. Phosphorylation of histone H3 during transcriptional activation depends on promoter structure.
    Genes Dev. 2003 Jan 1;17(1):43-8 PMID: 12514098
  23. Chromatin silencing: RNA in the driving seat.
    Curr Biol. 2003 Jan 8;13(1):R13-5 PMID: 12526757
  24. Chromosomal fragility in patients with triple A syndrome.
    Am J Med Genet A. 2003 Feb 15;117A(1):30-6 PMID: 12548737
  25. Histone and chromatin cross-talk.
    Curr Opin Cell Biol. 2003 Apr;15(2):172-83 PMID: 12648673
  26. RNAs templating chromatin structure for dosage compensation in animals.
    Bioessays. 2003 May;25(5):434-42 PMID: 12717814
  27. 5-Methylcytosine localised in mammalian constitutive heterochromatin.
    Nature. 1974 Oct 18;251(5476):636-7 PMID: 4609195
  28. Cell stress and translational inhibitors transiently increase the abundance of mammalian SINE transcripts.
    Nucleic Acids Res. 1995 May 25;23(10):1758-65 PMID: 7784180
  29. HSF1 granules: a novel stress-induced nuclear compartment of human cells.
    J Cell Sci. 1997 Dec;110 ( Pt 23):2925-34 PMID: 9359875
  30. HSF1 transcription factor concentrates in nuclear foci during heat shock: relationship with transcription sites.
    J Cell Sci. 1997 Dec;110 ( Pt 23):2935-41 PMID: 9359877
  31. Hsp70 and Hsp40 chaperone activities in the cytoplasm and the nucleus of mammalian cells.
    J Biol Chem. 1997 Dec 26;272(52):33283-9 PMID: 9407119
  32. Potential Alu function: regulation of the activity of double-stranded RNA-activated kinase PKR.
    Mol Cell Biol. 1998 Jan;18(1):58-68 PMID: 9418853
  33. Contribution of growing RNA molecules to the nuclear transcripts foci observed by FISH.
    Exp Cell Res. 1998 Jan 10;238(1):299-304 PMID: 9457084
  34. Growth-related changes in phosphorylation of yeast RNA polymerase II.
    J Biol Chem. 1998 Feb 20;273(8):4689-94 PMID: 9468530
  35. Molecular chaperones as HSF1-specific transcriptional repressors.
    Genes Dev. 1998 Mar 1;12(5):654-66 PMID: 9499401
  36. Is chromosome 9 loss a marker of disease recurrence in transitional cell carcinoma of the urinary bladder?
    Br J Cancer. 1998 Jun;77(12):2193-8 PMID: 9649132
  37. Induction of B2 RNA polymerase III transcription by heat shock: enrichment for heat shock induced sequences in rodent cells by hybridization subtraction.
    Nucleic Acids Res. 1986 Jul 25;14(14):5793-811 PMID: 2426659
  38. A method for the quantitative analysis of human heat shock gene expression using a multiplex RT-PCR assay.
    Cell Stress Chaperones. 1999 Sep;4(3):153-61 PMID: 10547064
  39. Physiological stresses increase mouse short interspersed element (SINE) RNA expression in vivo.
    Gene. 1999 Nov 1;239(2):367-72 PMID: 10548739
  40. Preparation of site-specific antibodies to acetylated histones.
    Methods. 1999 Nov;19(3):417-24 PMID: 10579937
  41. The HP1 protein family: getting a grip on chromatin.
    Curr Opin Genet Dev. 2000 Apr;10(2):204-10 PMID: 10753776
  42. Heat shock effects on cell cycle progression.
    Cell Mol Life Sci. 2000 Mar;57(3):450-63 PMID: 10823246
  43. Analysis of the mammalian heat-shock response. Inducible gene expression and heat-shock factor activity.
    Methods Mol Biol. 2000;99:217-55 PMID: 10909088
  44. Structure and dynamics of hnRNP-labelled nuclear bodies induced by stress treatments.
    J Cell Sci. 2000 Nov;113 ( Pt 22):4043-53 PMID: 11058091
  45. Phosphorylation of histone H3 correlates with transcriptionally active loci.
    Genes Dev. 2000 Dec 1;14(23):3003-13 PMID: 11114889
  46. X-chromosome inactivation: counting, choice and initiation.
    Nat Rev Genet. 2001 Jan;2(1):59-67 PMID: 11253071
  47. Roles of the heat shock transcription factors in regulation of the heat shock response and beyond.
    FASEB J. 2001 May;15(7):1118-31 PMID: 11344080
  48. Glycogen synthase kinase 3beta and extracellular signal-regulated kinase inactivate heat shock transcription factor 1 by facilitating the disappearance of transcriptionally active granules after heat shock.
    Mol Cell Biol. 1998 Nov;18(11):6624-33 PMID: 9774677
  49. The C-terminal region but not the Arg-X-Pro repeat of Epstein-Barr virus protein EB2 is required for its effect on RNA splicing and transport.
    J Virol. 1999 May;73(5):4090-100 PMID: 10196305
  50. Allelic losses at 1p, 9q, 10q, 14q, and 22q in the progression of aggressive meningiomas and undifferentiated meningeal sarcomas.
    Cancer Genet Cytogenet. 1999 Apr 15;110(2):103-10 PMID: 10214357
Article Info
Journal
The Journal of cell biology
Abbr.
J Cell Biol
ISSN
0021-9525
Published
2004-01-05
Epub
2003-00-29
Pages
25-33
Language
English
Region
United States
NLM ID
0375356
PMCID
PMC2171959
Subset
IM
Corrections
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