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Integrative Biological NMR

Andrew Atkinson & Olivier Saurel

Group Leaders

Our research focuses on the development of NMR and MD methods and their applications in structural biology and to the biophysics of membranes. We characterize pathogen-derived lipids and study their effects on pathogen or host membranes, and analyze intermolecular processes involving membrane proteins (ligand-receptor, metal transport), with a particular focus on mycobacterial infection.

The Integrative Biological NMR group applies its expertise and state-of-the-art equipment to pursue ambitious projects in structural biology with important implications in pharmacology. The structure, dynamics and interactions of biomolecules are the three pillars for elucidating biochemical processes at atomic resolution. NMR combined with MD simulations is ideally suited to the study of such processes. We continuously explore new avenues, such as the structure and function of complex membrane assemblies, and the influence of macromolecular dynamics on interactions, in the context of bacterial infection.


Structure, dynamics, and interactions of macromolecules, with a focus on membrane proteins.
In recent years, we have characterized the internal dynamics of OmpA from Klebsiella pneumoniae in liposomes using fast-MAS solid state NMR (2017, JACS). In the high impact field of G protein-coupled receptors (GPCRs), we determined the structures and characterized the dynamics of dynorphin and ghrelin agonists bound to KOR and GHSR receptors, respectively (2015, 2019, PNAS).

Our current research focuses on understanding key molecular processes involved in Mycobacterium tuberculosis (Mtb) infection and the defence mechanisms developed by Mtb in macrophages. Host membrane proteins include receptors for which ligand binding at the cell surface leads to activation of intracellular signaling pathways. We are currently studying the human C-lectin Mincle to understand its interactions with glycolipids from Mtb that contribute to mycobacterial virulence and stimulate the host immune system.

The transmembrane signaling mechanisms are poorly understood but are thought to involve interactions with the FcRgamma receptor. We are seeking to characterize these interactions experimentally and using MD simulations.
Human macrophages respond to Mtb infection by raising the concentration of zinc ions to levels that are toxic to the mycobacterium. To counteract this response, mycobacterial metallochaperones coupled to metal efflux pumps of the P-type ATPase superfamily of membrane-bound proteins act to reduce the metal ion concentration. We are studying the molecular mechanisms involved in the interaction of the metallochaperone Zmc with the P-type ATPase CtpC (collaboration with O. Neyrolles, IPBS).

Biophysics of membranes, with a focus on the Mtb envelope.

Mycobacterial lipids constitute the building blocks of the extremely thick mycobacterial envelope which constitutes a diffusion barrier to drugs, thus contributing to Mtb persistence. In addition to binding to host receptors such as Mincle, they also serve as virulence factors acting on the host membrane, causing damage and modulating the immune response. We are investigating the structure and dynamic of these lipids (e.g. DIM, 2019 PNAS) by solid-state NMR and MD simulations to decipher their role in Mtb infection.



Macromolecular interactions by NMR : Solution structure of the THAP zinc finger of THAP1 in complex with its DNA target (PDB entry 2KO0).

© Olivier Saurel


Main Publications

Ferré et al. (2019) Structure and dynamics of G protein-coupled receptor-bound ghrelin reveal the critical role of the octanoyl chain. Proc Natl Acad Sci USA


Augenstreich et al. (2019) The conical shape of DIM lipids promotes Mycobacterium tuberculosis infection of macrophages. Proc Natl Acad Sci USA


Gervais et al. (2018) Small molecule-based targeting of TTD-A dimerization to control TFIIH transcriptional activity represents a potential strategy for anticancer therapy. J Biol Chem


Saurel et al. (2017) Local and global dynamics in Klebsiella pneumoniae Outer membrane protein A in lipid bilayers probed at atomic resolution. J Am Chem Soc


Carrel et al. (2017) Identification of specific posttranslational O-mycoloylations mediating protein targeting to the mycomembrane. Proc Natl Acad Sci USA


Cukier et al. (2017) NMR secondary structure and interactions of recombinant human MOZART1 protein, a component of the gamma-tubulin complex. Protein Sci


Menchon et al. (2016) Structure-based virtual ligand screening on the XRCC4/DNA ligase IV interface. Sci Rep


O’Connor et al. (2015) NMR structure and dynamics of the agonist dynorphin peptide bound to the human kappa opioid receptor. Proc Natl Acad Sci USA



Andrew Atkinson

CNRS Senior Research Associate

Georges Czaplicki

Professor - University of Toulouse

Pascal Demange

CNRS Research director

Evert Haanappel

CNRS Research associate

Alain Milon

Professor - University of Toulouse

Isabelle Muller

Associate Professor - University of Toulouse

Valerie Réat

CNRS Research associate

Olivier Saurel

CNRS Engineer

Research Assistants

Nathalie Doncescu

CNRS Engineer

Pascal Ramos

University of Toulouse Engineer


  • Schahl, A., Gerber, I.C., Réat, V., and Jolibois, F. Diversity of the hydrogen bond network and its impact on NMR parameters of amylose B polymorph: a study using molecular dynamics and DFT calculations within periodic boundary conditions. J Phys Chem B, 125, 158-168 (2021).


  • Atkinson, R.A. NMR of proteins and nucleic acids. In Nuclear Magnetic Resonance: Volume 46 , ed. P. Hodgkinson, Royal Society of Chemistry (2020).
  • Dekoninck, K., Létoquart, J., Laguri, C., Demange, P., Bevernaegie, R., Simorre, J.P., Dehu, O., Iorga, B.I., Elias, B., Cho, S.H., and Collet, J.F. Defining the function of OmpA in the Rcs stress response. Elife, 9:e60861 (2020).
  • Del Toro, D., Carrasquero-Ordaz, M.A., Chu, A., Ruff, T., Shahin, M., Jackson, V.A., Chavent, M., Berbeira-Santana, M., Seyit-Bremer, G., Brignani, S., Kaufmann, R., Lowe, E., Klein, R., and Seiradake, E. Structural basis of teneurin-latrophilin interaction in repulsive guidance of migrating neurons. Cell, 180, 323-339.e19 (2020).
  • Fontaine, C., Buscato, M., Vinel, A., Giton, F., Raymond-Letron, I., Kim, S.H., Katzenellenbogen, B.S., Katzenellenbogen, J.A., Gourdy, P., Milon, A., Flouriot, G., Ohlsson, C., Lenfant, F., and Arnal, J.F. The tissue-specific effects of different 17beta-estradiol doses reveal the key sensitizing role of AF1 domain in ERalpha activity. Mol Cell Endocrinol, 505:110741 (2020).
  • Martinez, X., Chavent, M., and Baaden, M. Visualizing protein structures - tools and trends. Biochem Soc Trans, 48, 499–506 (2020).
  • Nguyen, M.C., Saurel, O., Carivenc, C., Gavalda, S., Saitta, S., Tran, M.P., Milon, A., Chalut, C., Guilhot, C., Mourey, L., and Pedelacq, J.-D. Conformational flexibility of coenzyme A and its impact on the post-translational modification of acyl carrier proteins by 4’-phosphopantetheinyl transferases. FEBS J, 287, 4729-4746 (2020).
  • Schahl, A., Réat, V. and Jolibois, F. Structures and NMR spectra of short amylose-lipid complexes. Insight using molecular dynamics and DFT quantum chemical calculations. Carbohydr Polym, 235:115846 (2020).


  • Abraham, M., Apostolov, R., Barnoud, J., Bauer, P., Blau, C., Bonvin, A.M.J.J., Chavent, M., Chodera, J., Čondić-Jurkić, K., Delemotte, L., Grubmüller, H., Howard, R.J., Jordan, E.J., Lindahl, E., Ollila, O.H.S., Selent, J., Smith, D.G.A., Stansfeld, P.J., Tiemann, J.K.S., Trellet, M., Woods, C., and Zhmurov, A. Sharing data from molecular simulations. J Chem Inf Model, 59, 4093–4099 (2019).
  • Augenstreich, J., Haanappel, E., Ferré, G., Czaplicki, G., Jolibois, F., Destainville, N., Guilhot, C., Milon, A., Astarie-Dequeker, C., and Chavent, M. The conical shape of DIM lipids promotes Mycobacterium tuberculosis infection of macrophages. Proc Natl Acad Sci USA, 116, 25649-25658 (2019).
  • Ferré, G., Louet, M., Saurel, O., Delort, B., Czaplicki, G., M'Kadmi, C., Damian, M., Renault, P., Cantel, S., Gavara, L., Demange, P., Marie, J., Fehrentz, J.A., Floquet, N., Milon, A., and Banères, J.L. Structure and dynamics of G protein-coupled receptor-bound ghrelin reveal the critical role of the octanoyl chain. Proc Natl Acad Sci USA, 116, 17525-17530 (2019).
  • Ferré, G., Czaplicki, G., Demange, P., and Milon, A. Structure and dynamics of dynorphin peptide and its receptor. Vitam Horm, 111, 17–47 (2019).
  • Guillet, V., Bordes, P., Bon, C., Marcoux, J., Gervais, V., Sala, A.J., Dos Reis, S., Slama, N., Mares-Mejía, I., Cirinesi, A.-M., Maveyraud, L., Genevaux, P., and Mourey, L. Structural insights into chaperone addiction of toxin-antitoxin systems. Nat Commun, 10:782 (2019).
  • Hedger, G., Koldsø, H., Chavent, M., Siebold, C., Rohatgi, R., and Sansom, M.S.P. Cholesterol interaction sites on the transmembrane domain of the Hedgehog signal transducer and class F G protein-coupled receptor Smoothened. Structure, 27, 549-559 (2019).
  • Kotras, C., Fossépré, M., Roger, M., Gervais, V., Richeter, S., Gerbier, P., Ulrich, S., Surin, M., and Clément, S. A cationic tetraphenylethene as a light-up supramolecular probe for DNA G-quadruplexes. Front Chem, 7:493 (2019).
  • Ladurantie, C., Coustets, M., Czaplicki, G., Demange, P., Mazères, S., Dauvillier, S., Teissié, J., Rols, M.-P., Milon, A., Ecochard, V., Gross, G., and Paquereau, L. A protein nanocontainer targeting epithelial cancers: rational engineering, biochemical characterization, drug loading and cell delivery. Nanoscale, 11, 3248–3260 (2019).
  • Martinez, X., Krone, M., Alharbi, N., Rose, A.S., Laramee, R.S., O’Donoghue, S., Baaden, M., and Chavent, M. Molecular graphics: bridging structural biologists and computer scientists. Structure, 27, 1617–1623 (2019).


  • Drozdz, W., Walczak, A., Bessin, Y., Gervais, V., Cao, X. Y., Lehn, J. M., Ulrich, S., and Stefankiewicz, A. R. (2018) Multivalent metallosupramolecular assemblies as effective DNA binding agents, Chemistry.
  • Drozdz, W., Bessin, Y., Gervais, V., Cao, X. Y., Lehn, J. M., Stefankiewicz, A. R., and Ulrich, S. (2018) Switching Multivalent DNA Complexation using Metal-Controlled Cationic Supramolecular Self-Assemblies, Chemistry 24, 1518-1521.


  • Duncan, A. L., Reddy, T., Koldso, H., Helie, J., Fowler, P. W., Chavent, M., and Sansom, M. S. P. (2017) Protein crowding and lipid complexity influence the nanoscale dynamic organization of ion channels in cell membranes, Sci Rep-Uk 7.
  • Cukier, C. D., Tourdes, A., El-Mazouni, D., Guillet, V., Nomme, J., Mourey, L., Milon, A., Merdes, A., and Gervais, V. (2017) NMR secondary structure and interactions of recombinant human MOZART1 protein, a component of the gamma-tubulin complex, Protein Sci 26, 2240-2248.
  • Carel, C., Marcoux, J., Reat, V., Parra, J., Latge, G., Laval, F., Demange, P., Burlet-Schiltz, O., Milon, A., Daffe, M., Tropis, M. G., and Renault, M. A. M. (2017) Identification of specific posttranslational O-mycoloylations mediating protein targeting to the mycomembrane, Proc. Natl. Acad. Sci. USA 114, 4231-4236.
  • Saurel, O., Iordanov, I., Nars, G., Demange, P., Le Marchand, T., Andreas, L. B., Pintacuda, G., and Milon, A., Local and Global Dynamics in Klebsiella pneumoniae Outer Membrane Protein a in Lipid Bilayers Probed at Atomic Resolution, J.A.C.S. 139, 1590-1597 (2017).

Download the complete list of publications from 2016 to 2002

Collaborations inside France

  • L. Mourey, M. Daffé, M. Tropis, P. Calsou, O. Cuvillier, IPBS, University of Toulouse – CNRS
  • M. Remaud-Siméon, A. Marty, I. André, R. Fauré, M. J. O’Donohue, LISBP, University of Toulouse – INRA - CNRS
  • J. F. Arnal, I2MC, University of Toulouse – INSERM
  • J.L. Banères, IBMM, Montpellier
  • S. Granier, IGF, Montpellier
  • G. Pintacuda, CRMN, Lyon


International Collaborations

  • M. Baldus, Utrecht University, The Netherlands
  • L. Eggeling, IBG-1, Jülich, Germany
  • V. Cherezov and R. Stevens, USC, Los Angeles, USA
  • K. Wüthrich, The Scripps Research Institute, La Jolla, USA
  • J.A. Bengoechea, Queen’s University, Belfast, UK