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How order and disorder within paramyxoviral nucleoproteins and phosphoproteins orchestrate the molecular interplay of transcription and replication

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Abstract

In this review, we summarize computational and experimental data gathered so far showing that structural disorder is abundant within paramyxoviral nucleoproteins (N) and phosphoproteins (P). In particular, we focus on measles, Nipah, and Hendra viruses and highlight both commonalities and differences with respect to the closely related Sendai virus. The molecular mechanisms that control the disorder-to-order transition undergone by the intrinsically disordered C-terminal domain (NTAIL) of their N proteins upon binding to the C-terminal X domain (XD) of the homologous P proteins are described in detail. By having a significant residual disorder, NTAIL–XD complexes are illustrative examples of “fuzziness”, whose possible functional significance is discussed. Finally, the relevance of N–P interactions as promising targets for innovative antiviral approaches is underscored, and the functional advantages of structural disorder for paramyxoviruses are pinpointed.

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Acknowledgements

S.L. wishes to thank all the members of her lab and her co-workers for their critical contribution to the studies herein summarized. Within her group, she thanks David Karlin, François Ferron, Jean-Marie Bourhis, Kenth Johansson, Antoine Gruet, Johnny Habchi, David Blocquel, Jenny Erales, Lorenzo Baronti, Marion Dosnon, Jennifer Roche and Matilde Beltrandi (previous members), and Christophe Bignon (present members). The authors also wish to thank David Blocquel who is the author of Fig. 9c. Among her numerous past and present co-workers, she thanks Bruno Canard (AFMB, Marseille, France), Maria Maté (AFMB, Marseille, France), Michael Oglesbee (Ohio State University, Columbus, USA), Hélène Valentin (CIRI, Lyon, France), Valerie Belle and Bruno Guigliarelli (BIP, Marseille, France), Janez Strancar (Jozef Stefan Institute, Ljubljana, Slovenia), Gary Daughdrill (University of South Florida, USA), Martin Blackledge, Malene Ringkjobin-Jensen and Guillaume Communie (Institut de Biologie Structurale, Grenoble, France), Jin Wang (Changchun Institute of Applied Chemistry, Chinese Academy of Sciences, Changchun, China), Roberta Pierattelli and Isabella Felli (CERM, Florence, Italy), Rita Grandori (Universita’ degli Studi Milano-Bicocca, Milan, Italy), Andrea Cavalli (IRB, Bellinzona, Switzerland), Pascale Barbier (CRO2 UMR_S911, Marseille, France), Paolo Carloni (Institute for Advanced Simulation IAS-5 and Institute of Neuroscience and Medicine INM-9, Jülich, Germany), Joanna Brunel (CIRI, Lyon, France), Daniela Bonetti (Sapienza, Universita’ of Rome, Italy), and Carlo Camilloni and Michele Vendruscolo (Department of Chemistry, University of Cambridge, UK). She is particularly grateful to Vladimir Uversky (University of South Florida, USA) for the numerous stimulating discussions and for his useful advice on various issues. The studies herein reviewed were carried out with the financial support of the Agence Nationale de la Recherche, specific programs “Physico-Chimie du Vivant”, ANR-08-PCVI-0020-01, and “ASTRID”, ANR-11-ASTR-003-01 to S.L and D.G. They also benefited from support from the CNRS, the Direction Générale de l’Armement (DGA) and the Fondation pour la Recherche Médicale (FRM). Work partly supported by grants from the Italian Ministero dell’Istruzione dell’Università e della Ricerca (Progetto di Interesse ‘Invecchiamento’ to S.G.) and Sapienza University of Rome (C26A155S48 to S.G). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

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Authors and Affiliations

  1. Aix-Marseille Univ, AFMB UMR 7257, 163, avenue de Luminy, Case 932, 13288, Marseille Cedex 09, France

    Sonia Longhi

  2. CNRS, AFMB UMR 7257, 13288, Marseille, France

    Sonia Longhi

  3. CIRI, International Center for Infectiology Research, Université de Lyon, Lyon, France

    Louis-Marie Bloyet & Denis Gerlier

  4. INSERM, U1111, Lyon, France

    Louis-Marie Bloyet & Denis Gerlier

  5. Ecole Normale Supérieure de Lyon, Lyon, France

    Louis-Marie Bloyet & Denis Gerlier

  6. Université Claude Bernard Lyon 1, Centre International de Recherche en Infectiologie, Lyon, France

    Louis-Marie Bloyet & Denis Gerlier

  7. CNRS, UMR5308, Lyon, France

    Louis-Marie Bloyet & Denis Gerlier

  8. Istituto Pasteur, Fondazione Cenci Bolognetti and Istituto di Biologia e Patologia Molecolari del CNR, Dipartimento di Scienze Biochimiche “A. Rossi Fanelli”, Sapienza Università di Roma, 00185, Rome, Italy

    Stefano Gianni

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Correspondence to Sonia Longhi.

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Longhi, S., Bloyet, LM., Gianni, S. et al. How order and disorder within paramyxoviral nucleoproteins and phosphoproteins orchestrate the molecular interplay of transcription and replication. Cell. Mol. Life Sci. 74, 3091–3118 (2017). https://doi.org/10.1007/s00018-017-2556-3

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