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J. Biol. Chem., Vol. 281, Issue 44, 33704-33716, November 3, 2006

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Structural and Mutational Analysis of Human Ad37 and Canine Adenovirus 2 Fiber Heads in Complex with the D1 Domain of Coxsackie and Adenovirus Receptor^*

Elena Seiradake¹, Hugues Lortat-Jacob, Olivier Billet^¶||**2, Eric J. Kremer^¶||**3, and Stephen Cusack⁴

From the Grenoble Outstation, European Molecular Biology Laboratory, Grenoble, France, Institut de Biologie Structurale, Unité Mixte de Recherche (UMR) 5075 Commissariat à l'Energie Atomique-CNRS-Université Joseph Fourier, Grenoble, France, ^¶Institut de Génétique Moléculaire de Montpellier, ^||CNRS UMR 5535, and ^**Institut Fédératif de Recherche 122, 34293 Montpellier, France

Adenovirus fibers from most serotypes bind the D1 domain of coxsackie and adenovirus receptor (CAR), although the binding residues are not strictly conserved. To understand this further, we determined the crystal structures of canine adenovirus serotype 2 (CAV-2) and the human adenovirus serotype 37 (HAd37) in complex with human CAR D1 at 2.3 and 1.5Å resolution, respectively. Structure comparison with the HAd12 fiber head-CAR D1 complex showed that the overall topology of the interaction is conserved but that the interfaces differ in number and identity of interacting residues, shape complementarity, and degree of conformational adaptation. Using surface plasmon resonance, we characterized the binding affinity to CAR D1 of wild type and mutant CAV-2 and HAd37 fiber heads. We found that CAV-2 has the highest affinity but fewest direct interactions, with the reverse being true for HAd37. Moreover, we found that conserved interactions can have a minor contribution, whereas serotype-specific interactions can be essential. These results are discussed in the light of virus evolution and design of adenovirus vectors for gene transfer.

Received for publication, June 2, 2006 , and in revised form, August 21, 2006.

The atomic coordinates and structure factors (code 2J12, 2j2j, 2j1k) have been deposited in the Protein Data Bank, Research Collaboratory for Structural Bioinformatics, Rutgers University, New Brunswick, NJ (http://www.rcsb.org/).

^* Part of this work was funded by the Association Française contre les Myopathies (AFM) and the Vaincre les Maladies Lysosomales. The costs of publication of this article were defrayed in part by the payment of page charges. This article must therefore be hereby marked "advertisement"in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

¹ Supported by an EU FP6 Marie Curie Early Stage Research Training Fellowship under Contract MEST-CT-2004-504640 ("E-STAR").

² An AFM postdoctoral fellow.

³ An INSERM Director of Research. To whom correspondence may be addressed: IGMM, CNRS UMR 5535, 1919 Route de Mende, 34293 Montpellier, France. Tel.: 33467613672; E-mail: eric.kremer{at}igmm.cnrs.fr.

⁴ To whom correspondence may be addressed: Grenoble Outstation, European Molecular Biology Laboratory, 6 rue Jules Horowitz, BP181, 38042 Grenoble Cedex 9, France. Fax: 33476207199; Tel.: 33476207238; E-mail: cusack{at}embl-grenoble.fr.

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