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Cooperative interactions between odorant-binding proteins of Anopheles gambiae

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Abstract

To understand olfactory discrimination in Anopheles gambiae, we made six purified recombinant OBPs and investigated their ligand-binding properties. All OBPs were expressed in bacteria with additional production of OBP47 in the yeast Kluveromyces lactis. Ligand-binding experiments, performed with a diverse set of organic compounds, revealed marked differences between the OBPs. Using the fluorescent probe N-phenyl-1-naphthylamine, we also measured the binding curves for binary mixtures of OBPs and obtained, in some cases, unexpected behaviour, which could only be explained by the OBPs forming heterodimers with binding characteristics different from those of the component proteins. This shows that OBPs in mosquitoes can form complexes with novel ligand specificities, thus amplifying the repertoire of OBPs and the number of semiochemicals that can be discriminated. Confirmation of the likely role of heterodimers was demonstrated by in situ hybridisation, suggesting that OBP1 and OBP4 are co-expressed in some antennal sensilla of A. gambiae.

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Abbreviations

OBP:

Odorant-binding protein

MALDI-TOF:

Matrix-assisted laser desorption ionisation-time of flight

ESI-MS:

Electrospray ionisation mass spectrometry

FITC:

Phenyl-isothiocyanate

1-NPN:

N-phenyl-1-naphthylamine

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Acknowledgments

We thank Drs. Dan Woods (Inscent, Inc., Irvine, CA) and Marika Walter (University of California, Irvine, CA) for access to their A. gambiae antennal cDNA library, which was used as starting material for the isolation of the ORFs of the OBPs analysed in this report. We also thank Maria Calzetta for technical assistance in rearing and manipulation of mosquito samples. This study was supported by a European Union grant (FP7/2007-2013,Grant Agreement No. FP7-222927) to FRD, JK, KI, LF and PP.

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Authors and Affiliations

  1. Department of Biology and Agricultural Plants, University of Pisa, Via S. Michele, 4, 56124, Pisa, Italy

    Huili Qiao & Paolo Pelosi

  2. Department of Biological Chemistry, Rothamsted Research, Harpenden, UK

    Xiaoli He, Liping Ban, Linda Field & Jing-Jiang Zhou

  3. Institute of Physiology, University of Hohenheim, Stuttgart, Germany

    Danuta Schymura & Jürgen Krieger

  4. Centro Interdipartimentale di Spettrometria di Massa, University of Firenze, Florence, Italy

    Francesca Romana Dani & Elena Michelucci

  5. Dipartimento di Scienze di Sanità Pubblica, Istituto Pasteur-Fondazione Cenci-Bolognetti, Sezione di Parassitologia, University ‘Sapienza’, Rome, Italy

    Beniamino Caputo & Alessandra della Torre

  6. Insect Molecular Genetics and Biotechnology Group, Institute of Biology, National Centre for Scientific Research ‘Demokritos’, Athens, Greece

    Kostas Iatrou

Authors
  1. Huili Qiao
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  2. Xiaoli He
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  9. Alessandra della Torre
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  11. Jing-Jiang Zhou
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  13. Paolo Pelosi
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Corresponding authors

Correspondence to Jing-Jiang Zhou or Paolo Pelosi.

Additional information

Dedicated to the memory of the late Harald Biessmann, our colleague and dear friend, who completed the cloning and initial characterization of the majority of Anopheles gambiae odorant-binding proteins.

H. Qiao and X. He contributed equally to the work.

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18_2010_539_MOESM1_ESM.tif

Figure S1. Electrophoretic separation in native conditions of refolded samples of An. gambiae OBP1, OBP3, OBP4. Their migration as single bands indicates that refolding has not produced more than one form, nor oligomeric structures (TIFF 941 kb)

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Qiao, H., He, X., Schymura, D. et al. Cooperative interactions between odorant-binding proteins of Anopheles gambiae . Cell. Mol. Life Sci. 68, 1799–1813 (2011). https://doi.org/10.1007/s00018-010-0539-8

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