Complexity and Diversity of the Mammalian Sialome Revealed by Nidovirus Virolectins
Martijn A. Langereis,
Mark J.G. Bakkers,
Lingquan Deng,
Vered Padler-Karavani,
Stephin J. Vervoort,
Ruben J.G. Hulswit,
Arno L.W. van Vliet,
Gerrit J. Gerwig,
Stefanie A.H. de Poot,
Willemijn Boot,
Anne Marie van Ederen,
Balthasar A. Heesters,
Chris M. van der Loos,
Frank J.M. van Kuppeveld,
Hai Yu,
Eric G. Huizinga,
Xi Chen,
Ajit Varki,
Johannis P. Kamerling,
Raoul J. de Groot
Affiliations
Martijn A. Langereis
Virology Division, Department of Infectious Diseases and Immunology, Faculty of Veterinary Medicine, Utrecht University, 3584 CL Utrecht, the Netherlands
Mark J.G. Bakkers
Virology Division, Department of Infectious Diseases and Immunology, Faculty of Veterinary Medicine, Utrecht University, 3584 CL Utrecht, the Netherlands
Lingquan Deng
Glycobiology Research and Training Center, Departments of Medicine and Cellular and Molecular Medicine, University of California, San Diego, La Jolla, CA 92093-0687, USA
Vered Padler-Karavani
Glycobiology Research and Training Center, Departments of Medicine and Cellular and Molecular Medicine, University of California, San Diego, La Jolla, CA 92093-0687, USA
Stephin J. Vervoort
Virology Division, Department of Infectious Diseases and Immunology, Faculty of Veterinary Medicine, Utrecht University, 3584 CL Utrecht, the Netherlands
Ruben J.G. Hulswit
Virology Division, Department of Infectious Diseases and Immunology, Faculty of Veterinary Medicine, Utrecht University, 3584 CL Utrecht, the Netherlands
Arno L.W. van Vliet
Virology Division, Department of Infectious Diseases and Immunology, Faculty of Veterinary Medicine, Utrecht University, 3584 CL Utrecht, the Netherlands
Gerrit J. Gerwig
Bio-Organic Chemistry, Bijvoet Center for Biomolecular Research, Faculty of Sciences, Utrecht University, 3584 CH Utrecht, the Netherlands
Stefanie A.H. de Poot
Virology Division, Department of Infectious Diseases and Immunology, Faculty of Veterinary Medicine, Utrecht University, 3584 CL Utrecht, the Netherlands
Willemijn Boot
Virology Division, Department of Infectious Diseases and Immunology, Faculty of Veterinary Medicine, Utrecht University, 3584 CL Utrecht, the Netherlands
Anne Marie van Ederen
Department of Pathobiology, Faculty of Veterinary Medicine, Utrecht University, 3584 CL Utrecht, the Netherlands
Balthasar A. Heesters
Virology Division, Department of Infectious Diseases and Immunology, Faculty of Veterinary Medicine, Utrecht University, 3584 CL Utrecht, the Netherlands
Chris M. van der Loos
Department of Cardiovascular Pathology, Free University Amsterdam, 1105 AZ Amsterdam, the Netherlands
Frank J.M. van Kuppeveld
Virology Division, Department of Infectious Diseases and Immunology, Faculty of Veterinary Medicine, Utrecht University, 3584 CL Utrecht, the Netherlands
Hai Yu
Department of Chemistry, University of California, Davis, Davis, CA 95616, USA
Eric G. Huizinga
Crystal and Structural Chemistry, Bijvoet Center for Biomolecular Research, Faculty of Sciences, Utrecht University, 3584 CH Utrecht, the Netherlands
Xi Chen
Department of Chemistry, University of California, Davis, Davis, CA 95616, USA
Ajit Varki
Glycobiology Research and Training Center, Departments of Medicine and Cellular and Molecular Medicine, University of California, San Diego, La Jolla, CA 92093-0687, USA
Johannis P. Kamerling
Bio-Organic Chemistry, Bijvoet Center for Biomolecular Research, Faculty of Sciences, Utrecht University, 3584 CH Utrecht, the Netherlands
Raoul J. de Groot
Virology Division, Department of Infectious Diseases and Immunology, Faculty of Veterinary Medicine, Utrecht University, 3584 CL Utrecht, the Netherlands
Sialic acids (Sias), 9-carbon-backbone sugars, are among the most complex and versatile molecules of life. As terminal residues of glycans on proteins and lipids, Sias are key elements of glycotopes of both cellular and microbial lectins and thus act as important molecular tags in cell recognition and signaling events. Their functions in such interactions can be regulated by post-synthetic modifications, the most common of which is differential Sia-O-acetylation (O-Ac-Sias). The biology of O-Ac-Sias remains mostly unexplored, largely because of limitations associated with their specific in situ detection. Here, we show that dual-function hemagglutinin-esterase envelope proteins of nidoviruses distinguish between a variety of closely related O-Ac-Sias. By using soluble forms of hemagglutinin-esterases as lectins and sialate-O-acetylesterases, we demonstrate differential expression of distinct O-Ac-sialoglycan populations in an organ-, tissue- and cell-specific fashion. Our findings indicate that programmed Sia-O-acetylation/de-O-acetylation may be critical to key aspects of cell development, homeostasis, and/or function.