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And Stuart M. Haslam G. Busch, Anne Dell, Christopher W Glycobiology and Extracellular Matrices: Glycan Analysis and Influenza A Virus Infection of Primary Swine Respiratory Epithelial Cells: THE IMPORTANCE OF NeuAc α2−6 GLYCANS Allen C. Bateman, Rositsa Karamanska, Marc G. Busch, Anne Dell, Christopher W. Olsen Downloaded from and Stuart M. Haslam J. Biol. Chem. 2010, 285:34016-34026. doi: 10.1074/jbc.M110.115998 originally published online August 19, 2010 http://www.jbc.org/ Access the most updated version of this article at doi: 10.1074/jbc.M110.115998 Find articles, minireviews, Reflections and Classics on similar topics on the JBC Affinity Sites. at Imperial College London on September 19, 2014 Alerts: • When this article is cited • When a correction for this article is posted Click here to choose from all of JBC's e-mail alerts Supplemental material: http://www.jbc.org/content/suppl/2010/09/08/M110.115998.DC1.html This article cites 55 references, 25 of which can be accessed free at http://www.jbc.org/content/285/44/34016.full.html#ref-list-1 THE JOURNAL OF BIOLOGICAL CHEMISTRY VOL. 285, NO. 44, pp. 34016–34026, October 29, 2010 Author’s Choice © 2010 by The American Society for Biochemistry and Molecular Biology, Inc. Printed in the U.S.A. Glycan Analysis and Influenza A Virus Infection of Primary Swine Respiratory Epithelial Cells THE IMPORTANCE OF NeuAc␣2–6 GLYCANS*□S Received for publication, February 19, 2010, and in revised form, August 18, 2010 Published, JBC Papers in Press, August 19, 2010, DOI 10.1074/jbc.M110.115998 Allen C. Bateman‡§1, Rositsa Karamanska¶1, Marc G. Busch‡2, Anne Dell¶, Christopher W. Olsen‡3, and Stuart M. Haslam¶4 From the ‡Department of Pathobiological Sciences, School of Veterinary Medicine, and §Cellular and Molecular Biology Graduate Program, University of Wisconsin-Madison, Madison, Wisconsin 53706 and the ¶Division of Molecular Biosciences, Faculty of Natural Sciences, Biochemistry Building, Imperial College London, South Kensington Campus, London SW7 2AZ, United Kingdom To better understand influenza virus infection of pigs, we Influenza A viruses are significant pathogens of many spe- examined primary swine respiratory epithelial cells (SRECs, the cies, including humans and pigs. Pigs have long been postulated Downloaded from primary target cells of influenza viruses in vivo), as a model sys- as intermediate hosts in the generation of pandemic human tem. Glycomic profiling of SRECs by mass spectrometry influenza viruses because they are susceptible to human and revealed a diverse range of glycans terminating in sialic acid or avian viruses (1–6). Since the late 1990s, influenza viruses in Gal␣Gal. In terms of sialylation, ␣2–6 linkage was more abun- North American pigs have evolved extensively, with the emer- dant than ␣2–3, and NeuAc was more abundant than NeuGc. gence of “triple reassortant” H3N2 (rH3N2) viruses that con- Virus binding and infection experiments were conducted to tain genes from human-, avian-, and swine-lineage viruses http://www.jbc.org/ determine functionally important glycans for influenza virus (7–9). Further reassortment with existing viruses led to the infection, with a focus on recently emerged swine viruses. Infec- development of H1N1, H1N2, H3N1, and H2N3 reassortant tion of SRECs with swine and human viruses resulted in differ- viruses in North American pigs (10–13). Finally, at some point ent infectivity levels. Glycan microarray analysis with a high in past years, North American triple reassortant and Eurasian infectivity “triple reassortant” virus ((A/Swine/MN/593/99 swine viruses underwent reassortment to create the human at Imperial College London on September 19, 2014 (H3N2)) that spread widely throughout the North American pandemic 2009 H1N1 influenza virus (14–16). These events swine population and a lower infectivity human virus isolated document the natural occurrence of genetic reassortment from a single pig (A/Swine/ONT/00130/97 (H3N2)) showed among influenza viruses in pigs, demonstrate the importance of that both viruses bound exclusively to glycans containing pigs in the epidemiology and evolution of influenza viruses for NeuAc␣2–6, with strong binding to sialylated polylactosamine humans, and emphasize the need for a better understanding of and sialylated N-glycans. Treatment with mannosamine precur- influenza virus infection of pigs. sors of sialic acid (to alter NeuAc/NeuGc abundances) and To determine what allowed the initial rH3N2 viruses to suc- linkage-specific sialidases prior to infection indicated that the cessfully emerge, spread, and be maintained in the swine pop- influenza viruses tested preferentially utilize NeuAc␣2–6-sialy- ulation, we previously compared a representative rH3N2 virus lated glycans to infect SRECs. Our data indicate that NeuAc␣2– (A/Swine/Minnesota/593/99 (Sw/MN)) with a human-lineage 6-terminated polylactosamine and sialylated N-glycans are virus (A/Swine/Ontario/00130/97 (Sw/ONT)) isolated from a important determinants for influenza viruses to infect SRECs. single pig during the same time period. Sw/MN was more infec- As NeuAc␣2–6 polylactosamine glycans play major roles in tious for pigs in vivo (17), and it infected a significantly higher human virus infection, the importance of these receptor compo- number of cultured primary swine respiratory epithelial cells nents in virus infection of swine cells has implications for trans- (SRECs,5 the target cells of influenza viruses in pigs) (18). mission of viruses between humans and pigs and for pigs as pos- Finally, using reverse genetics-generated Sw/MN ϫ Sw/ONT sible adaptation hosts of novel human influenza viruses. reassortant and point mutant viruses, we demonstrated that the infectivity phenotypes in SRECs were strongly dependent upon three amino acids within the viral HA (hemagglutinin) gene * This work was supported, in whole or in part, by National Institutes of Health (18). Grant R01 AI060646 (to C. W. O.). This work was also supported by Grant Influenza viruses initiate infection via the virus HA protein 082098 from the Wellcome Trust (to S. M. H. and A. D.). binding to host cell sialic acids (Sia) typically linked ␣2–3 or Author’s Choice—Final version full access. □S The on-line version of this article (available at http://www.jbc.org) contains ␣2–6 to galactose (Gal). Binding preference is widely believed supplemental Tables S1–S5 and Figs. S1–S5. to be a major determinant of influenza virus host range and 1 Both authors contributed equally to this work. 2 species specificity, because avian viruses preferentially bind Present address: Biology Dept., Drake University, Des Moines, IA. ␣ ␣ 3 To whom correspondence may be addressed: School of Veterinary Medicine, Sia 2–3Gal, whereas human and swine viruses bind Sia 2– University of Wisconsin-Madison, 2015 Linden Dr., Madison, WI 53706. Tel.: 608-263-5819; Fax: 608-890-1774; E-mail: [email protected]. 4 To whom correspondence may be addressed: Division of Molecular Bio- 5 The abbreviations used are: SREC, swine respiratory epithelial cell; NeuGc, sciences, Faculty of Natural Sciences, Biochemistry Bldg., Imperial College Lon- N-glycolylneuraminic acid; MDCK, Madin-Darby canine kidney cells; BEGM, don, South Kensington Campus, London, SW7 2AZ, United Kingdom. Tel.: bronchial epithelial cell growth media; ManNAc, N-acetylmannosamine; 4420-75945222; Fax: 4420-72250458; E-mail: [email protected]. ManNGc, N-glycolylmannosamine. 34016 JOURNAL OF BIOLOGICAL CHEMISTRY VOLUME 285•NUMBER 44•OCTOBER 29, 2010 Glycan Analysis and Influenza Virus Infection of Swine Cells 6Gal (19–22). However, in addition to the Sia-Gal linkage, Sia (18). Briefly, aseptically collected distal swine tracheal speci- species may influence virus infection and host range restriction mens were rinsed with phosphate-buffered saline (PBS) and (23). The main Sia species expressed in quail and chicken intes- placed in a Pronase/DNase tissue-dissociation solution for 72 h tine (the site of influenza virus replication in these species) is at 4 °C. Cells were then incubated at 37 °C in uncoated cell N-acetylneuraminic acid (NeuAc) (24), whereas affinity for culture dishes for 2 to 6 h, and nonadherent (epithelial) cells N-glycolylneuraminic acid (NeuGc)␣2–3Gal is important for were collected and seeded into type VI collagen (Sigma)-coated virus replication in the intestinal tract of mallard ducks (25). cell culture flasks (adherent fibroblasts were discarded). SRECs The human respiratory tract expresses solely NeuAc. (Humans were grown in serum-free, hormone-supplemented bronchial lack expression of NeuGc because of a mutation in the CMAH epithelial cell growth media (BEGM௡, Lonza, Walkersville, gene required to convert NeuAc into NeuGc (26).) Both NeuAc MD) and maintained at 37 °C in a 5% CO2 atmosphere up to and NeuGc are present in swine trachea (27), but the relative passage five. The collection and use of SRECs was approved functional importance of NeuAc versus NeuGc for infection of by the Animal Care and Use Committee of the School of pigs is not fully understood. Furthermore, recent data indicate Veterinary Medicine, University of Wisconsin-Madison. that influenza virus/receptor interactions are more complex The following viruses were used in this study: A/Brazil/ than the simple ␣2–3 versus ␣2–6 dichotomy would suggest 1137/99 (H1N1) and A/Brazil/02/99 (H3N2) human isolates (28). Finally, overall glycan topology is important for virus and A/Swine/MN/593/99 (triple reassortant H3N2) (34), Downloaded from binding and transmission (29, 30). In light of all these findings, A/Swine/ONT/00130/97 (human-lineage swine H3N2 iso- we sought to more fully understand the nature of glycans late) (34), A/Swine/NC/44173/00 (classical swine H1N1), expressed on SRECs and to examine influenza virus infection of and A/Swine/IND/9K035/99 (triple reassortant H1N2) (35) this novel swine cell system, with a focus on the reassortant swine isolates. Viruses were grown in MDCK cells, and virus viruses that have emerged and spread throughout the North titrations were performed in MDCK cells, and 50% tissue http://www.jbc.org/ American swine population over the past decade.
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