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DNA Physical Properties and Nucleosome Positions Are Major Determinants of HIV-1 Integrase Selectivity

Author

Listed:
  • Monica Naughtin
  • Zofia Haftek-Terreau
  • Johan Xavier
  • Sam Meyer
  • Maud Silvain
  • Yan Jaszczyszyn
  • Nicolas Levy
  • Vincent Miele
  • Mohamed Salah Benleulmi
  • Marc Ruff
  • Vincent Parissi
  • Cédric Vaillant
  • Marc Lavigne

Abstract

Retroviral integrases (INs) catalyse the integration of the reverse transcribed viral DNA into the host cell genome. This process is selective, and chromatin has been proposed to be a major factor regulating this step in the viral life cycle. However, the precise underlying mechanisms are still under investigation. We have developed a new in vitro integration assay using physiologically-relevant, reconstituted genomic acceptor chromatin and high-throughput determination of nucleosome positions and integration sites, in parallel. A quantitative analysis of the resulting data reveals a chromatin-dependent redistribution of the integration sites and establishes a link between integration sites and nucleosome positions. The co-activator LEDGF/p75 enhanced integration but did not modify the integration sites under these conditions. We also conducted an in cellulo genome-wide comparative study of nucleosome positions and human immunodeficiency virus type-1 (HIV-1) integration sites identified experimentally in vivo. These studies confirm a preferential integration in nucleosome-covered regions. Using a DNA mechanical energy model, we show that the physical properties of DNA probed by IN binding are important in determining IN selectivity. These novel in vitro and in vivo approaches confirm that IN has a preference for integration into a nucleosome, and suggest the existence of two levels of IN selectivity. The first depends on the physical properties of the target DNA and notably, the energy required to fit DNA into the IN catalytic pocket. The second depends on the DNA deformation associated with DNA wrapping around a nucleosome. Taken together, these results indicate that HIV-1 IN is a shape-readout DNA binding protein.

Suggested Citation

  • Monica Naughtin & Zofia Haftek-Terreau & Johan Xavier & Sam Meyer & Maud Silvain & Yan Jaszczyszyn & Nicolas Levy & Vincent Miele & Mohamed Salah Benleulmi & Marc Ruff & Vincent Parissi & Cédric Vaill, 2015. "DNA Physical Properties and Nucleosome Positions Are Major Determinants of HIV-1 Integrase Selectivity," PLOS ONE, Public Library of Science, vol. 10(6), pages 1-28, June.
  • Handle: RePEc:plo:pone00:0129427
    DOI: 10.1371/journal.pone.0129427
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    References listed on IDEAS

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    1. Anton Valouev & Steven M. Johnson & Scott D. Boyd & Cheryl L. Smith & Andrew Z. Fire & Arend Sidow, 2011. "Determinants of nucleosome organization in primary human cells," Nature, Nature, vol. 474(7352), pages 516-520, June.
    2. Mickaël Lelek & Nicoletta Casartelli & Danilo Pellin & Ermanno Rizzi & Philippe Souque & Marco Severgnini & Clelia Di Serio & Thomas Fricke & Felipe Diaz-Griffero & Christophe Zimmer & Pierre Charneau, 2015. "Chromatin organization at the nuclear pore favours HIV replication," Nature Communications, Nature, vol. 6(1), pages 1-12, May.
    3. Goedele N. Maertens & Stephen Hare & Peter Cherepanov, 2010. "The mechanism of retroviral integration from X-ray structures of its key intermediates," Nature, Nature, vol. 468(7321), pages 326-329, November.
    4. Bruna Marini & Attila Kertesz-Farkas & Hashim Ali & Bojana Lucic & Kamil Lisek & Lara Manganaro & Sandor Pongor & Roberto Luzzati & Alessandra Recchia & Fulvio Mavilio & Mauro Giacca & Marina Lusic, 2015. "Nuclear architecture dictates HIV-1 integration site selection," Nature, Nature, vol. 521(7551), pages 227-231, May.
    5. Eran Segal & Yvonne Fondufe-Mittendorf & Lingyi Chen & AnnChristine Thåström & Yair Field & Irene K. Moore & Ji-Ping Z. Wang & Jonathan Widom, 2006. "A genomic code for nucleosome positioning," Nature, Nature, vol. 442(7104), pages 772-778, August.
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