FREE SHIPPING over $40
OVER 10000 FIVE-STAR REVIEWS
5% OFF ALL SUBSCRIPTIONS
100% HAPPINESS GUARANTEE
Analyze Diet
0
Journal of virology2000; 74(24); 11825-11831; doi: 10.1128/jvi.74.24.11825-11831.2000

Sialic acid species as a determinant of the host range of influenza A viruses.

Abstract: The distribution of sialic acid (SA) species varies among animal species, but the biological role of this variation is largely unknown. Influenza viruses differ in their ability to recognize SA-galactose (Gal) linkages, depending on the animal hosts from which they are isolated. For example, human viruses preferentially recognize SA linked to Gal by the alpha2,6(SAalpha2,6Gal) linkage, while equine viruses favor SAalpha2,3Gal. However, whether a difference in relative abundance of specific SA species (N-acetylneuraminic acid [NeuAc] and N-glycolylneuraminic acid [NeuGc]) among different animals affects the replicative potential of influenza viruses is uncertain. We therefore examined the requirement for the hemagglutinin (HA) for support of viral replication in horses, using viruses whose HAs differ in receptor specificity. A virus with an HA recognizing NeuAcalpha2,6Gal but not NeuAcalpha2,3Gal or NeuGcalpha2,3Gal failed to replicate in horses, while one with an HA recognizing the NeuGcalpha2,3Gal moiety replicated in horses. Furthermore, biochemical and immunohistochemical analyses and a lectin-binding assay demonstrated the abundance of the NeuGcalpha2,3Gal moiety in epithelial cells of horse trachea, indicating that recognition of this moiety is critical for viral replication in horses. Thus, these results provide evidence of a biological effect of different SA species in different animals.
Get Full Text
Publication Date: 2000-11-23 PubMed ID: 11090182PubMed Central: PMC112465DOI: 10.1128/jvi.74.24.11825-11831.2000Google Scholar: Lookup
The Equine Research Bank provides access to a large database of publicly available scientific literature. Inclusion in the Research Bank does not imply endorsement of study methods or findings by Mad Barn.
LinkedInCopy
  • Journal Article
  • Research Support
  • Non-U.S. Gov't
  • Research Support
  • U.S. Gov't
  • P.H.S.

Summary

This research summary has been generated with artificial intelligence and may contain errors and omissions. Refer to the original study to confirm details provided. Submit correction.

The research article explores the role of different sialic acid (SA) species in determining the host range for influenza A viruses. Focusing on the relation between variants of these SA species found in different animals and the replication potential for the flu virus, the study uncovers a biological effect of different SA species in different animals.

Understanding Sialic Acid Varieties and Their Role

  • The SA species’ distribution shows variation among different animal species. However, their biological significance had been largely unknown until this research.
  • Influenza viruses have a differing ability to recognize combinations of SA and galactose (Gal), depending on the animal species they originate from.
  • For instance, human viruses best identify SA linked to Gal via an alpha2,6(SAalpha2,6Gal) linkage. Simultaneously, equine viruses favor an SAalpha2,3Gal variant.

Examining Sialic Acid Impact on Viral Replication

  • The study aimed to determine whether the relative abundance of specific SA species affected influenza viruses’ replication.
  • The SA species under examination included N-acetylneuraminic acid [NeuAc] and N-glycolylneuraminic acid [NeuGc].
  • The research utilized different viruses whose hemagglutinin (HA), a surface protein facilitating viral entry into the host cell, had different receptor specificities in horses.

Key Findings: Host-Specific Sialic Acid Influence

  • The study found that a virus with an HA identifying the NeuAcalpha2,6Gal variant, but not the NeuAcalpha2,3Gal or NeuGcalpha2,3Gal, failed to replicate in horses.
  • Conversely, a virus with an HA that recognized the NeuGcalpha2,3Gal function successfully replicated in the host.
  • Additional biochemical and immunohistochemical analyses reinforced that the NeuGcalpha2,3Gal moiety is abundant in the epithelial cells of a horse’s trachea.
  • Consequently, the study concluded that the recognition of the NeuGcalpha2,3Gal moiety is crucial for the influenza viruses to replicate in horses.
  • This concludes that different sialic acid species in different animals indeed impact the potential for viral replication, thus influencing the host range of the influenza virus.

Cite This Article

APA
Suzuki Y, Ito T, Suzuki T, Holland RE, Chambers TM, Kiso M, Ishida H, Kawaoka Y. (2000). Sialic acid species as a determinant of the host range of influenza A viruses. J Virol, 74(24), 11825-11831. https://doi.org/10.1128/jvi.74.24.11825-11831.2000

Publication

Journal of virology
ISSN: 0022-538X
NlmUniqueID: 0113724
Country: United States
Language: English
Volume: 74
Issue: 24
Pages: 11825-11831

Researcher Affiliations

Suzuki, Y
  • Department of Biochemistry, School of Pharmaceutical Sciences, University of Shizuoka, Yada, Shizuoka-shi 422-8526, Japan.
Ito, T
    Suzuki, T
      Holland, R E
        Chambers, T M
          Kiso, M
            Ishida, H
              Kawaoka, Y

                MeSH Terms

                • Animals
                • Humans
                • Influenza A virus / physiology
                • Influenza, Human / metabolism
                • Influenza, Human / virology
                • N-Acetylneuraminic Acid / metabolism
                • Species Specificity
                • Virus Replication

                References

                This article includes 52 references
                1. Baum LG, Paulson JC. The N2 neuraminidase of human influenza virus has acquired a substrate specificity complementary to the hemagglutinin receptor specificity.. Virology 1991 Jan;180(1):10-5.
                  pubmed: 1984642doi: 10.1016/0042-6822(91)90003-tgoogle scholar: lookup
                2. Bean WJ Jr, Sriram G, Webster RG. Electrophoretic analysis of iodine-labeled influenza virus RNA segments.. Anal Biochem 1980 Feb;102(1):228-32.
                  pubmed: 7356157doi: 10.1016/0003-2697(80)90343-7google scholar: lookup
                3. Beare AS, Webster RG. Replication of avian influenza viruses in humans.. Arch Virol 1991;119(1-2):37-42.
                  pubmed: 1863223doi: 10.1007/bf01314321google scholar: lookup
                4. Chambers TM, Shortridge KF, Li PH, Powell DG, Watkins KL. Rapid diagnosis of equine influenza by the Directigen FLU-A enzyme immunoassay.. Vet Rec 1994 Sep 17;135(12):275-9.
                  pubmed: 7817505doi: 10.1136/vr.135.12.275google scholar: lookup
                5. Claas EC, Osterhaus AD, van Beek R, De Jong JC, Rimmelzwaan GF, Senne DA, Krauss S, Shortridge KF, Webster RG. Human influenza A H5N1 virus related to a highly pathogenic avian influenza virus.. Lancet 1998 Feb 14;351(9101):472-7.
                  pubmed: 9482438doi: 10.1016/s0140-6736(97)11212-0google scholar: lookup
                6. Connor RJ, Kawaoka Y, Webster RG, Paulson JC. Receptor specificity in human, avian, and equine H2 and H3 influenza virus isolates.. Virology 1994 Nov 15;205(1):17-23.
                  pubmed: 7975212doi: 10.1006/viro.1994.1615google scholar: lookup
                7. Couceiro JN, Paulson JC, Baum LG. Influenza virus strains selectively recognize sialyloligosaccharides on human respiratory epithelium; the role of the host cell in selection of hemagglutinin receptor specificity.. Virus Res 1993 Aug;29(2):155-65.
                  pubmed: 8212857doi: 10.1016/0168-1702(93)90056-sgoogle scholar: lookup
                8. Fujii Y, Higashi H, Ikuta K, Kato S, Naiki M. Specificities of human heterophilic Hanganutziu and Deicher (H-D) antibodies and avian antisera against H-D antigen-active glycosphingolipids.. Mol Immunol 1982 Jan;19(1):87-94.
                  pubmed: 6176858doi: 10.1016/0161-5890(82)90250-4google scholar: lookup
                9. Guo Y, Wang M, Kawaoka Y, Gorman O, Ito T, Saito T, Webster RG. Characterization of a new avian-like influenza A virus from horses in China.. Virology 1992 May;188(1):245-55.
                  pubmed: 1314452doi: 10.1016/0042-6822(92)90754-dgoogle scholar: lookup
                10. Haesebrouck F, Pensaert M. Influenza in swine in Belgium (1969-1986): epizootiologic aspects.. Comp Immunol Microbiol Infect Dis 1988;11(3-4):215-22.
                  pubmed: 2851410doi: 10.1016/0147-9571(88)90040-9google scholar: lookup
                11. Hara S, Takemori Y, Yamaguchi M, Nakamura M, Ohkura Y. Fluorometric high-performance liquid chromatography of N-acetyl- and N-glycolylneuraminic acids and its application to their microdetermination in human and animal sera, glycoproteins, and glycolipids.. Anal Biochem 1987 Jul;164(1):138-45.
                  pubmed: 3674364doi: 10.1016/0003-2697(87)90377-0google scholar: lookup
                12. Higa HH, Rogers GN, Paulson JC. Influenza virus hemagglutinins differentiate between receptor determinants bearing N-acetyl-, N-glycollyl-, and N,O-diacetylneuraminic acids.. Virology 1985 Jul 15;144(1):279-82.
                  pubmed: 4060591doi: 10.1016/0042-6822(85)90325-3google scholar: lookup
                13. Hinshaw VS, Webster RG, Naeve CW, Murphy BR. Altered tissue tropism of human-avian reassortant influenza viruses.. Virology 1983 Jul 15;128(1):260-3.
                  pubmed: 6880029doi: 10.1016/0042-6822(83)90337-9google scholar: lookup
                14. Hirabayashi Y, Suzuki T, Suzuki Y, Taki T, Matsumoto M, Higashi H, Kato S. A new method for purification of anti-glycosphingolipid antibody. Avian anti-hematoside (NeuGc) antibody.. J Biochem 1983 Jul;94(1):327-30.
                  pubmed: 6619119doi: 10.1093/oxfordjournals.jbchem.a134350google scholar: lookup
                15. Hirabayashi Y, Higashi H, Kato S, Taniguchi M, Matsumoto M. Occurrence of tumor-associated ganglioside antigens with Hanganutziu-Deicher antigenic activity on human melanomas.. Jpn J Cancer Res 1987 Jun;78(6):614-20.
                  pubmed: 3112076
                16. Ito T, Couceiro JN, Kelm S, Baum LG, Krauss S, Castrucci MR, Donatelli I, Kida H, Paulson JC, Webster RG, Kawaoka Y. Molecular basis for the generation in pigs of influenza A viruses with pandemic potential.. J Virol 1998 Sep;72(9):7367-73.
                  pmc: PMC109961pubmed: 9696833doi: 10.1128/jvi.72.9.7367-7373.1998google scholar: lookup
                17. Ito T, Suzuki Y, Suzuki T, Takada A, Horimoto T, Wells K, Kida H, Otsuki K, Kiso M, Ishida H, Kawaoka Y. Recognition of N-glycolylneuraminic acid linked to galactose by the alpha2,3 linkage is associated with intestinal replication of influenza A virus in ducks.. J Virol 2000 Oct;74(19):9300-5.
                  pmc: PMC102129pubmed: 10982377doi: 10.1128/jvi.74.19.9300-9305.2000google scholar: lookup
                18. Katz JM, Wang M, Webster RG. Direct sequencing of the HA gene of influenza (H3N2) virus in original clinical samples reveals sequence identity with mammalian cell-grown virus.. J Virol 1990 Apr;64(4):1808-11.
                  pmc: PMC249319pubmed: 2319652doi: 10.1128/jvi.64.4.1808-1811.1990google scholar: lookup
                19. Kawaoka Y, Krauss S, Webster RG. Avian-to-human transmission of the PB1 gene of influenza A viruses in the 1957 and 1968 pandemics.. J Virol 1989 Nov;63(11):4603-8.
                  pmc: PMC251093pubmed: 2795713doi: 10.1128/jvi.63.11.4603-4608.1989google scholar: lookup
                20. Kida H, Yanagawa R, Matsuoka Y. Duck influenza lacking evidence of disease signs and immune response.. Infect Immun 1980 Nov;30(2):547-53.
                  pmc: PMC551346pubmed: 7439994doi: 10.1128/iai.30.2.547-553.1980google scholar: lookup
                21. Kida H, Ito T, Yasuda J, Shimizu Y, Itakura C, Shortridge KF, Kawaoka Y, Webster RG. Potential for transmission of avian influenza viruses to pigs.. J Gen Virol 1994 Sep;75 ( Pt 9):2183-8.
                  pubmed: 8077918doi: 10.1099/0022-1317-75-9-2183google scholar: lookup
                22. KLENK E, LEMPFRID H. [The nature of cell receptors for the influenza virus].. Hoppe Seylers Z Physiol Chem 1957;307(2-6):278-83.
                  pubmed: 13448658
                23. KLENK E, UHLENBRUCK G. [A neuraminic acidcontaining mucoprotein from cattle erythrocyte stroma].. Hoppe Seylers Z Physiol Chem 1958;311(4-6):227-33.
                  pubmed: 13598384
                24. Laver WG, Webster RG. Studies on the origin of pandemic influenza. 3. Evidence implicating duck and equine influenza viruses as possible progenitors of the Hong Kong strain of human influenza.. Virology 1973 Feb;51(2):383-91.
                  pubmed: 4632653doi: 10.1016/0042-6822(73)90437-6google scholar: lookup
                25. Mancini G, Donatelli I, Rozera C, Arangio Ruiz G, Buttò S. Antigenic and biochemical analysis of influenza "A" H3N2 viruses isolated from pigs.. Arch Virol 1985;83(3-4):157-67.
                  pubmed: 3155941doi: 10.1007/bf01309913google scholar: lookup
                26. Martensson E, Raal A, Svennerholm L. Sialic acid in blood serum. Biochim Biophys Acta 1958;301:24–129.
                27. Matrosovich M, Zhou N, Kawaoka Y, Webster R. The surface glycoproteins of H5 influenza viruses isolated from humans, chickens, and wild aquatic birds have distinguishable properties.. J Virol 1999 Feb;73(2):1146-55.
                  pmc: PMC103935pubmed: 9882316doi: 10.1128/jvi.73.2.1146-1155.1999google scholar: lookup
                28. Murphy BR, Hinshaw VS, Sly DL, London WT, Hosier NT, Wood FT, Webster RG, Chanock RM. Virulence of avian influenza A viruses for squirrel monkeys.. Infect Immun 1982 Sep;37(3):1119-26.
                  pmc: PMC347656pubmed: 7129631doi: 10.1128/iai.37.3.1119-1126.1982google scholar: lookup
                29. Naiki M. Chemical and immunochemical properties of two classes of globoside from equine organs.. Jpn J Exp Med 1971 Feb;41(1):67-81.
                  pubmed: 4994225
                30. Ottis K, Sidoli L, Bachmann PA, Webster RG, Kaplan MM. Human influenza A viruses in pigs: isolation of a H3N2 strain antigenically related to A/England/42/72 and evidence for continuous circulation of human viruses in the pig population.. Arch Virol 1982;73(2):103-8.
                  pubmed: 6184032doi: 10.1007/bf01314719google scholar: lookup
                31. PETTERSSON SO, SIVERTSSON R, SJOGREN S, SVENNERHOLM L. The sialic acids of hog pancreas.. Biochim Biophys Acta 1958 May;28(2):444-5.
                  pubmed: 13535748doi: 10.1016/0006-3002(58)90498-0google scholar: lookup
                32. Rogers GN, Paulson JC. Receptor determinants of human and animal influenza virus isolates: differences in receptor specificity of the H3 hemagglutinin based on species of origin.. Virology 1983 Jun;127(2):361-73.
                  pubmed: 6868370doi: 10.1016/0042-6822(83)90150-2google scholar: lookup
                33. Rogers GN, D'Souza BL. Receptor binding properties of human and animal H1 influenza virus isolates.. Virology 1989 Nov;173(1):317-22.
                  pubmed: 2815586doi: 10.1016/0042-6822(89)90249-3google scholar: lookup
                34. Rota PA, Rocha EP, Harmon MW, Hinshaw VS, Sheerar MG, Kawaoka Y, Cox NJ, Smith TF. Laboratory characterization of a swine influenza virus isolated from a fatal case of human influenza.. J Clin Microbiol 1989 Jun;27(6):1413-6.
                  pmc: PMC267575pubmed: 2754013doi: 10.1128/jcm.27.6.1413-1416.1989google scholar: lookup
                35. Schauer R. Chemistry, metabolism, and biological functions of sialic acids.. Adv Carbohydr Chem Biochem 1982;40:131-234.
                  pubmed: 6762816doi: 10.1016/s0065-2318(08)60109-2google scholar: lookup
                36. Schauer R. Sialic acids: chemistry, metabolism, and function. New York, N.Y: Springer; 1982.
                37. Scholtissek C, Rohde W, Von Hoyningen V, Rott R. On the origin of the human influenza virus subtypes H2N2 and H3N2.. Virology 1978 Jun 1;87(1):13-20.
                  pubmed: 664248doi: 10.1016/0042-6822(78)90153-8google scholar: lookup
                38. Scholtissek C, Bürger H, Kistner O, Shortridge KF. The nucleoprotein as a possible major factor in determining host specificity of influenza H3N2 viruses.. Virology 1985 Dec;147(2):287-94.
                  pubmed: 2416114doi: 10.1016/0042-6822(85)90131-xgoogle scholar: lookup
                39. Snyder MH, Buckler-White AJ, London WT, Tierney EL, Murphy BR. The avian influenza virus nucleoprotein gene and a specific constellation of avian and human virus polymerase genes each specify attenuation of avian-human influenza A/Pintail/79 reassortant viruses for monkeys.. J Virol 1987 Sep;61(9):2857-63.
                  pmc: PMC255805pubmed: 2441080doi: 10.1128/jvi.61.9.2857-2863.1987google scholar: lookup
                40. Snyder MH, Clements ML, De Borde D, Maassab HF, Murphy BR. Attenuation of wild-type human influenza A virus by acquisition of the PA polymerase and matrix protein genes of influenza A/Ann Arbor/6/60 cold-adapted donor virus.. J Clin Microbiol 1985 Nov;22(5):719-25.
                  pmc: PMC268513pubmed: 4056002doi: 10.1128/jcm.22.5.719-725.1985google scholar: lookup
                41. Subbarao K, Klimov A, Katz J, Regnery H, Lim W, Hall H, Perdue M, Swayne D, Bender C, Huang J, Hemphill M, Rowe T, Shaw M, Xu X, Fukuda K, Cox N. Characterization of an avian influenza A (H5N1) virus isolated from a child with a fatal respiratory illness.. Science 1998 Jan 16;279(5349):393-6.
                  pubmed: 9430591doi: 10.1126/science.279.5349.393google scholar: lookup
                42. Subbarao EK, London W, Murphy BR. A single amino acid in the PB2 gene of influenza A virus is a determinant of host range.. J Virol 1993 Apr;67(4):1761-4.
                  pmc: PMC240216pubmed: 8445709doi: 10.1128/jvi.67.4.1761-1764.1993google scholar: lookup
                43. Suzuki T, Horiike G, Yamazaki Y, Kawabe K, Masuda H, Miyamoto D, Matsuda M, Nishimura SI, Yamagata T, Ito T, Kida H, Kawaoka Y, Suzuki Y. Swine influenza virus strains recognize sialylsugar chains containing the molecular species of sialic acid predominantly present in the swine tracheal epithelium.. FEBS Lett 1997 Mar 10;404(2-3):192-6.
                  pubmed: 9119062doi: 10.1016/s0014-5793(97)00127-0google scholar: lookup
                44. Suzuki Y, Matsunaga M, Matsumoto M. N-Acetylneuraminyllactosylceramide, GM3-NeuAc, a new influenza A virus receptor which mediates the adsorption-fusion process of viral infection. Binding specificity of influenza virus A/Aichi/2/68 (H3N2) to membrane-associated GM3 with different molecular species of sialic acid.. J Biol Chem 1985 Feb 10;260(3):1362-5.
                  pubmed: 3838173
                45. Suzuki Y, Nakao T, Ito T, Watanabe N, Toda Y, Xu G, Suzuki T, Kobayashi T, Kimura Y, Yamada A. Structural determination of gangliosides that bind to influenza A, B, and C viruses by an improved binding assay: strain-specific receptor epitopes in sialo-sugar chains.. Virology 1992 Jul;189(1):121-31.
                  pubmed: 1376537doi: 10.1016/0042-6822(92)90687-kgoogle scholar: lookup
                46. Tian SF, Buckler-White AJ, London WT, Reck LJ, Chanock RM, Murphy BR. Nucleoprotein and membrane protein genes are associated with restriction of replication of influenza A/Mallard/NY/78 virus and its reassortants in squirrel monkey respiratory tract.. J Virol 1985 Mar;53(3):771-5.
                  pmc: PMC254705pubmed: 3973966doi: 10.1128/jvi.53.3.771-775.1985google scholar: lookup
                47. Tůmová B, Vĕzníková D, Mensík J, Stumpa A. Surveillance of influenza in pig herds in Czechoslovakia in 1974--1979. 1. Introduction of influenza epidemic A (H3N2) viruses into pig herds.. Zentralbl Veterinarmed B 1980;27(7):517-23.
                  pubmed: 6161501
                48. Varki A. Diversity in the sialic acids.. Glycobiology 1992 Feb;2(1):25-40.
                  pmc: PMC7108601pubmed: 1550987doi: 10.1093/glycob/2.1.25google scholar: lookup
                49. Webster RG. Antigenic hybrids of influenza A viruses with surface antigens to order.. Virology 1970 Nov;42(3):633-42.
                  pubmed: 5529980doi: 10.1016/0042-6822(70)90309-0google scholar: lookup
                50. Webster RG, Bean WJ, Gorman OT, Chambers TM, Kawaoka Y. Evolution and ecology of influenza A viruses.. Microbiol Rev 1992 Mar;56(1):152-79.
                  pmc: PMC372859pubmed: 1579108doi: 10.1128/mr.56.1.152-179.1992google scholar: lookup
                51. Webster RG, Yakhno M, Hinshaw VS, Bean WJ, Murti KG. Intestinal influenza: replication and characterization of influenza viruses in ducks.. Virology 1978 Feb;84(2):268-78.
                  pmc: PMC7131577pubmed: 23604doi: 10.1016/0042-6822(78)90247-7google scholar: lookup
                52. Wibberley G, Swallow C, Roberts DH. Characterization of an influenza A (H3N2) virus isolated from pigs in England in 1987.. Br Vet J 1988 Mar-Apr;144(2):196-201.
                  pmc: PMC7130373pubmed: 2838122doi: 10.1016/0007-1935(88)90053-xgoogle scholar: lookup

                Citations

                This article has been cited 227 times.
                Subscribe to our newsletter
                Join 99,658 horse owners like you who receive our email updates on horse health and nutrition.