Structure and sialyllactose binding of the carboxy-terminal head domain of the fibre from a siadenovirus, Turkey adenovirus 3

Abhimanyu K. Singh, M. Álvaro Berbís, Mónika Z. Ballmann, Michelle Kilcoyne, Margarita Menéndez, Thanh H. Nguyen, Lokesh Joshi, F. Javier Cañada, Jesús Jiménez-Barbero, M. Benkó, B. Harrach, Mark J. Van Raaij

Research output: Contribution to journalArticle

10 Citations (Scopus)

Abstract

The virulent form of Turkey adenovirus 3 (TAdV-3), also known as Turkey hemorrhagic enteritis virus (THEV), is an economically important poultry pathogen, while the avirulent form is used as a vaccine. TAdV-3 belongs to the genus Siadenovirus. The carboxy-terminal region of its fibre does not have significant sequence similarity to any other adenovirus fibre heads of known structure. Two amino acid sequence differences between virulent and avirulent TAdV-3 map on the fibre head: where virulent TAdV-3 contains Ile354 and Thr376, avirulent TAdV-3 contains Met354 and Met376. We determined the crystal structures of the trimeric virulent and avirulent TAdV-3 fibre head domains at 2.2 Å resolution. Each monomer contains a beta-sandwich, which, surprisingly, resembles reovirus fibre head more than other adenovirus fibres, although the ABCJ-GHID topology is conserved in all. A beta-hairpin insertion in the C-strand of each trimer subunit embraces its neighbouring monomer. The avirulent and virulent TAdV-3 fibre heads are identical apart from the exact orientation of the beta-hairpin insertion. In vitro, sialyllactose was identified as a ligand by glycan microarray analysis, nuclear magnetic resonance spectroscopy, and crystallography. Its dissociation constant was measured to be in the mM range by isothermal titration calorimetry. The ligand binds to the side of the fibre head, involving amino acids Glu392, Thr419, Val420, Lys421, Asn422, and Gly423 binding to the sialic acid group. It binds slightly more strongly to the avirulent form. We propose that, in vivo, the TAdV-3 fibre may bind a sialic acid-containing cell surface component.

Original languageEnglish
Article numbere0139339
JournalPLoS One
Volume10
Issue number9
DOIs
Publication statusPublished - Sep 29 2015

Fingerprint

Turkey adenovirus A
Siadenovirus
dietary fiber
Head
Fibers
sialic acids
N-Acetylneuraminic Acid
Adenoviridae
Turkey Coronavirus
Monomers
Aviadenovirus
crystallography
Ligands
N-acetylneuraminoyllactose
Amino Acids
Poultry
Calorimetry
Crystallography
Reoviridae
calorimetry

ASJC Scopus subject areas

  • Agricultural and Biological Sciences(all)
  • Biochemistry, Genetics and Molecular Biology(all)
  • Medicine(all)

Cite this

Singh, A. K., Berbís, M. Á., Ballmann, M. Z., Kilcoyne, M., Menéndez, M., Nguyen, T. H., ... Van Raaij, M. J. (2015). Structure and sialyllactose binding of the carboxy-terminal head domain of the fibre from a siadenovirus, Turkey adenovirus 3. PLoS One, 10(9), [e0139339]. https://doi.org/10.1371/journal.pone.0139339

Structure and sialyllactose binding of the carboxy-terminal head domain of the fibre from a siadenovirus, Turkey adenovirus 3. / Singh, Abhimanyu K.; Berbís, M. Álvaro; Ballmann, Mónika Z.; Kilcoyne, Michelle; Menéndez, Margarita; Nguyen, Thanh H.; Joshi, Lokesh; Cañada, F. Javier; Jiménez-Barbero, Jesús; Benkó, M.; Harrach, B.; Van Raaij, Mark J.

In: PLoS One, Vol. 10, No. 9, e0139339, 29.09.2015.

Research output: Contribution to journalArticle

Singh, AK, Berbís, MÁ, Ballmann, MZ, Kilcoyne, M, Menéndez, M, Nguyen, TH, Joshi, L, Cañada, FJ, Jiménez-Barbero, J, Benkó, M, Harrach, B & Van Raaij, MJ 2015, 'Structure and sialyllactose binding of the carboxy-terminal head domain of the fibre from a siadenovirus, Turkey adenovirus 3', PLoS One, vol. 10, no. 9, e0139339. https://doi.org/10.1371/journal.pone.0139339
Singh, Abhimanyu K. ; Berbís, M. Álvaro ; Ballmann, Mónika Z. ; Kilcoyne, Michelle ; Menéndez, Margarita ; Nguyen, Thanh H. ; Joshi, Lokesh ; Cañada, F. Javier ; Jiménez-Barbero, Jesús ; Benkó, M. ; Harrach, B. ; Van Raaij, Mark J. / Structure and sialyllactose binding of the carboxy-terminal head domain of the fibre from a siadenovirus, Turkey adenovirus 3. In: PLoS One. 2015 ; Vol. 10, No. 9.
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abstract = "The virulent form of Turkey adenovirus 3 (TAdV-3), also known as Turkey hemorrhagic enteritis virus (THEV), is an economically important poultry pathogen, while the avirulent form is used as a vaccine. TAdV-3 belongs to the genus Siadenovirus. The carboxy-terminal region of its fibre does not have significant sequence similarity to any other adenovirus fibre heads of known structure. Two amino acid sequence differences between virulent and avirulent TAdV-3 map on the fibre head: where virulent TAdV-3 contains Ile354 and Thr376, avirulent TAdV-3 contains Met354 and Met376. We determined the crystal structures of the trimeric virulent and avirulent TAdV-3 fibre head domains at 2.2 {\AA} resolution. Each monomer contains a beta-sandwich, which, surprisingly, resembles reovirus fibre head more than other adenovirus fibres, although the ABCJ-GHID topology is conserved in all. A beta-hairpin insertion in the C-strand of each trimer subunit embraces its neighbouring monomer. The avirulent and virulent TAdV-3 fibre heads are identical apart from the exact orientation of the beta-hairpin insertion. In vitro, sialyllactose was identified as a ligand by glycan microarray analysis, nuclear magnetic resonance spectroscopy, and crystallography. Its dissociation constant was measured to be in the mM range by isothermal titration calorimetry. The ligand binds to the side of the fibre head, involving amino acids Glu392, Thr419, Val420, Lys421, Asn422, and Gly423 binding to the sialic acid group. It binds slightly more strongly to the avirulent form. We propose that, in vivo, the TAdV-3 fibre may bind a sialic acid-containing cell surface component.",
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AU - Menéndez, Margarita

AU - Nguyen, Thanh H.

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