A single-molecule view of transcription reveals convoys of RNA polymerases and multi-scale bursting

Katjana Tantale, Florian Mueller (), Alja Kozulic-Pirher, Annick Lesne, Jean-Marc Victor, Marie-Cécile Robert, Serena Capozi, Racha Chouaib, Volker Bäcker, Julio Mateos-Langerak, Xavier Darzacq, Christophe Zimmer, Eugenia Basyuk () and Edouard Bertrand ()
Additional contact information
Katjana Tantale: Institut de Génétique Moléculaire de Montpellier, CNRS UMR5535, 1919, route de Mende
Florian Mueller: Unité Imagerie et Modélisation, Institut Pasteur and CNRS UMR 3691, 28, rue du Docteur Roux
Alja Kozulic-Pirher: Institut de Génétique Moléculaire de Montpellier, CNRS UMR5535, 1919, route de Mende
Annick Lesne: Institut de Génétique Moléculaire de Montpellier, CNRS UMR5535, 1919, route de Mende
Jean-Marc Victor: Institut de Génétique Moléculaire de Montpellier, CNRS UMR5535, 1919, route de Mende
Marie-Cécile Robert: Institut de Génétique Moléculaire de Montpellier, CNRS UMR5535, 1919, route de Mende
Serena Capozi: Institut de Génétique Moléculaire de Montpellier, CNRS UMR5535, 1919, route de Mende
Racha Chouaib: Institut de Génétique Moléculaire de Montpellier, CNRS UMR5535, 1919, route de Mende
Volker Bäcker: BioCampus Montpellier, CNRS UMS3426, 141, rue de la Cardonille
Julio Mateos-Langerak: BioCampus Montpellier, CNRS UMS3426, 141, rue de la Cardonille
Xavier Darzacq: Ecole Normale Supérieure, CNRS UMR
Christophe Zimmer: Unité Imagerie et Modélisation, Institut Pasteur and CNRS UMR 3691, 28, rue du Docteur Roux
Eugenia Basyuk: Institut de Génétique Moléculaire de Montpellier, CNRS UMR5535, 1919, route de Mende
Edouard Bertrand: Institut de Génétique Moléculaire de Montpellier, CNRS UMR5535, 1919, route de Mende

Nature Communications, 2016, vol. 7, issue 1, 1-14

Abstract: Abstract Live-cell imaging has revealed unexpected features of gene expression. Here using improved single-molecule RNA microscopy, we show that synthesis of HIV-1 RNA is achieved by groups of closely spaced polymerases, termed convoys, as opposed to single isolated enzymes. Convoys arise by a Mediator-dependent reinitiation mechanism, which generates a transient but rapid succession of polymerases initiating and escaping the promoter. During elongation, polymerases are spaced by few hundred nucleotides, and physical modelling suggests that DNA torsional stress may maintain polymerase spacing. We additionally observe that the HIV-1 promoter displays stochastic fluctuations on two time scales, which we refer to as multi-scale bursting. Each time scale is regulated independently: Mediator controls minute-scale fluctuation (convoys), while TBP-TATA-box interaction controls sub-hour fluctuations (long permissive/non-permissive periods). A cellular promoter also produces polymerase convoys and displays multi-scale bursting. We propose that slow, TBP-dependent fluctuations are important for phenotypic variability of single cells.

Date: 2016
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DOI: 10.1038/ncomms12248

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