Abstract
Treatment of HeLa cells with a DNA topoisomerase I-specific inhibitor, camptothecin, results in rapid cessation of the synthesis of the 45S rRNA precursor. The inhibition of rRNA synthesis is reversible following drug removal and correlates with the presence of camptothecin-trapped topoisomerase I-DNA abortive complexes, which can be detected as topoisomerase I-linked DNA breaks upon lysis with sodium dodecyl sulfate. These breaks were found to be concentrated within the transcribed region of human rRNA genes. No such sites can be detected in the inactive human rRNA genes in mouse-human hybrid cells, suggesting a preferential association of topoisomerase I with actively transcribed genes. The distribution of RNA polymerase molecules along the transcription unit of human rRNA genes in camptothecin-treated HeLa cells, as assayed by nuclear run-on transcription, shows a graded decrease of the RNA polymerase density toward the 3' end of the transcription unit; the density is minimally affected near the 5' start of the transcription unit. These results suggest that DNA topoisomerase I is normally involved in the elongation step of transcription, especially when the transcripts are long, and that camptothecin interferes with this role.
MeSH Terms
Camptothecin/pharmacology
DNA Topoisomerases, Type I/metabolism
HeLa Cells/metabolism
Humans
Models, Genetic
RNA, Ribosomal/biosynthesis
Topoisomerase I Inhibitors
Transcription, Genetic/drug effects
Chemicals
RNA, Ribosomal
Topoisomerase I Inhibitors
DNA Topoisomerases, Type I
Camptothecin
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Zhang H
Department of Biological Chemistry, Johns Hopkins University, Baltimore, MD 21205.
Wang J C
Liu L F
References (21)
21 references, click to expand
-
Camptothecin induces protein-linked DNA breaks via mammalian DNA topoisomerase I.
J Biol Chem. 1985 Nov 25;260(27):14873-8
PMID: 2997227
-
Identification of DNA topoisomerase II as an intracellular target of antitumor epipodophyllotoxins in simian virus 40-infected monkey cells.
Cancer Res. 1985 Nov;45(11 Pt 2):5872-6
PMID: 2996763
-
Localization of specific topoisomerase I interactions within the transcribed region of active heat shock genes by using the inhibitor camptothecin.
Mol Cell Biol. 1987 Jan;7(1):141-8
PMID: 3031452
-
Need for DNA topoisomerase activity as a swivel for DNA replication for transcription of ribosomal RNA.
Nature. 1987 Mar 26-Apr 1;326(6111):414-6
PMID: 2436053
-
Role of DNA topoisomerase I in the transcription of supercoiled rRNA gene.
Proc Natl Acad Sci U S A. 1987 May;84(10):3185-8
PMID: 3033639
-
Camptothecin-induced in vivo topoisomerase I cleavages in the transcriptionally active tyrosine aminotransferase gene.
Cell. 1987 Sep 25;50(7):1109-17
PMID: 2887294
-
Supercoiling of the DNA template during transcription.
Proc Natl Acad Sci U S A. 1987 Oct;84(20):7024-7
PMID: 2823250
-
Mitotic spindle pulls but fails to separate chromosomes in type II DNA topoisomerase mutants: uncoordinated mitosis.
EMBO J. 1986 May;5(5):1003-10
PMID: 15957215
-
Ribosome formation is blocked by camptothecin, a reversible inhibitor of RNA synthesis.
Proc Natl Acad Sci U S A. 1971 Dec;68(12):3009-14
PMID: 5289246
-
Selective interruption of high molecular weight RNA synthesis in HeLa cells by camptothecin.
Nat New Biol. 1972 May 31;237(74):144-6
PMID: 4504193
-
Isolation of ribosomal gene chromatin.
Dev Biol. 1977 Feb;55(2):375-86
PMID: 557006
-
A topological model for transcription based on unwinding angle analysis of E. coli RNA polymerase binary, initiation and ternary complexes.
Cell. 1982 May;29(1):81-90
PMID: 6286146
-
A technique for radiolabeling DNA restriction endonuclease fragments to high specific activity.
Anal Biochem. 1983 Jul 1;132(1):6-13
PMID: 6312838
-
Stimulation of 3T3 cells induces transcription of the c-fos proto-oncogene.
Nature. 1984 Oct 4-10;311(5985):433-8
PMID: 6090941
-
Nonintercalative antitumor drugs interfere with the breakage-reunion reaction of mammalian DNA topoisomerase II.
J Biol Chem. 1984 Nov 10;259(21):13560-6
PMID: 6092381
-
The absence of a human-specific ribosomal DNA transcription factor leads to nucleolar dominance in mouse greater than human hybrid cells.
Mol Cell Biol. 1984 Jul;4(7):1306-12
PMID: 6095060
-
Drosophila DNA topoisomerase I is associated with transcriptionally active regions of the genome.
Proc Natl Acad Sci U S A. 1984 Nov;81(22):6958-62
PMID: 6095263
-
A high affinity topoisomerase I binding sequence is clustered at DNAase I hypersensitive sites in Tetrahymena R-chromatin.
Cell. 1985 Jun;41(2):541-51
PMID: 2985282
-
Eukaryotic type I topoisomerase is enriched in the nucleolus and catalytically active on ribosomal DNA.
EMBO J. 1985 May;4(5):1237-43
PMID: 2988941
-
DNA topoisomerases.
Annu Rev Biochem. 1985;54:665-97
PMID: 2992360
-
Topoisomerase I interacts with transcribed regions in Drosophila cells.
Cell. 1986 Feb 14;44(3):401-7
PMID: 3002635