Skip to main content
PMC home page
Elsevier - PMC COVID-19 Collection logoLink to Elsevier - PMC COVID-19 Collection
. 2002 Nov 12;25(1):145–153. doi: 10.1016/0168-1702(92)90106-J

Increased influenza A virus sialidase activity with N-acetyl-9-O-acetylneuraminic acid-containing substrates resulting from influenza C virus O-acetylesterase action☆

I Muñoz-Barroso a, A García-Sastre a, E Villar a, J-C Manuguerra b, C Hannoun b, JA Cabezas a,∗
PMCID: PMC7173336  PMID: 1413991

Abstract

Influenza virus type C (Johannesburg/1/66) was used as a source for the enzyme O-acetylesterase (EC 3.1.1.53) with several natural sialoglycoconjugates as substrates. The resulting products were immediately employed as substrates using influenza virus type A [(Singapore/6/86) (H1N1) or Shanghai/11/87 (H3N2)] as a source for sialidase (neuraminidase, EC 3.2.1.18). A significant increase in the percentage of sialic acid released was found when the O-acetyl group was cleaved by O-acetylesterase activity from certain substrates (bovine submandibular gland mucin, rat serum glycoproteins, human saliva glycoproteins, mouse erythrocyte stroma, chick embryonic brain gangliosides and bovine brain gangliosides). A common feature of all these substrates is that they contain N-acetyl-9-O-acetylneuraminic acid residues. By contrast, no significant increase in the release of sialic acid was detected when certain other substrates could not be de-O-acetylated by the action of influenza C esterase, either because they lacked O-acetylsialic acid (human glycophorin A, α1-acid glycoprotein from human serum, fetuin and porcine submandibular gland mucin) or because the 4-O-acetyl group was scarcely cleaved by the viral O-acetylesterase (equine submandibular gland mucin). The biological significance of these facts is discussed, relative to the infective capacity of influenza C virus.

Keywords: Influenza C virus, O-Acetylesterase, Sialidase, Neuraminidase, Glycoconjugates

Footnotes

☆

Part of the results of this paper was presented at the 8th Workshop of the European Study Group on Lysosomal Diseases held in October, 1991, in Annecy, France.

References

  1. Aminoff D. Methods for the quantitative estimation of N-acetylneuraminic acid and their application to hydrolysates of sialomucoids. Biochem. J. 1961;81:384–392. doi: 10.1042/bj0810384. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Blumenfeld O.O., Adamany A. Vol. 75. 1978. Structural polymorphism within the amino-terminal region of MM, NN, and MN glycoproteins (glycophorins) of the human erythrocyte membrane; pp. 2727–2731. (Proc. Natl. Acad. Sci. USA). [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Cabezas J.A. Some questions and suggestions on the type references of the official nomenclature (IUB) for sialidase(s) and endosialidase. Biochem. J. 1991;278:311–312. doi: 10.1042/bj2780311. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Cabezas J.A., Vázquez-Porto J., Frois M.a.D., Marino C., Arzúa J. Acidos siálicos. III. Contenido en ácido siálico y en osas de la saliva humana. Rev. Esp. Fisiol. 1964;20:77–82. [PubMed] [Google Scholar]
  5. Cabezas J.A., Calvo P., Eid P., Martín J., Perez N., Reglero A., Rodrigo M., Hannoun C. Studies on neuraminidase from influenza virus A(H3N2) obtained by two procedures. Int. J. Biochem. 1982;14:311–319. doi: 10.1016/0020-711x(82)90092-1. [DOI] [PubMed] [Google Scholar]
  6. Cabezas J.A., Reglero A., Hannoun C. A fluorometric procedure for measuring the neuraminidase activity: its application to the determination of this activity in influenza and parainfluenza viruses. Anal. Biochem. 1983;131:121–126. doi: 10.1016/0003-2697(83)90142-2. [DOI] [PubMed] [Google Scholar]
  7. Cabezas J.A., Villar E., García-Sastre A., Manuguerra J.C., Hannoun C. New data on influenza virus type C confirm its peculiarities as a new genus. Intervirology. 1991;32:325–326. doi: 10.1159/000150216. [DOI] [PubMed] [Google Scholar]
  8. Dubois C., Manuguerra J.C., Hauttecoeur B., Maze J. Monoclonal antibody A2B5, which detects cell surface antigens, binds to ganglioside GT3 (II3 (NeuAc)3LacCer) and to its 9-O-acetylated derivate. J. Biol. Chem. 1990;265:2797–2803. [PubMed] [Google Scholar]
  9. Dykes A.C., Cherry J.D., Nolan C.E. A clinical, epidemiologic, serologie, and virologie study of influenza C virus infection. Arch. Intern. Med. 1980;140:1295–1298. [PubMed] [Google Scholar]
  10. Faillard H., Cabezas J.A. Isolieurung von N-acetyl- und N-Glykolyl-neuraminsäure aus Kälber und Hühnerserum. Hoppe-Seyler's Z. Physiol. Chem. 1963;333:266–271. doi: 10.1515/bchm2.1963.333.1.266. [DOI] [PubMed] [Google Scholar]
  11. Gahmberg C.G., Jokinen M., Karhi K.K., Kämpe O., Peterson P.A., Anderson L.C. Glycophorin A: in vitro biogenesis and processing. Meth. Enzymol. 1983;96:281–296. doi: 10.1016/s0076-6879(83)96026-3. [DOI] [PubMed] [Google Scholar]
  12. García-Sastre A., Villar E., Manuguerra J.C., Hannoun C., Cabezas J.A. Activity of influenza C virus O-acetylesterase with O-acetyl-containing compounds. Biochem. J. 1991;273:435–441. doi: 10.1042/bj2730435. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Gerber P., Woolridge R.L., Seal J.R., Ziegra S.R. Vol. 81. 1952. Epidemie influenza B and C in Navy recruits during winter of 1951-52; pp. 624–628. (Proc. Soc. Expo. Biol. Med.). [DOI] [PubMed] [Google Scholar]
  14. Gottschalk A., Bhargava A.S. Submaxillary gland glycoproteins. In: Gottschalk A., editor. Vol. B. Elsevier; Amsterdam: 1972. pp. 810–829. (Glycoproteins). [Google Scholar]
  15. Herder G., Klenk H.-D. The surface receptor is a major determinant of the all tropism of influenza C virus. Virology. 1987;159:102–108. doi: 10.1016/0042-6822(87)90352-7. [DOI] [PubMed] [Google Scholar]
  16. Herrler G., Compans R.W., Meier-Ewert H. A precursor glycoprotein in influenza C virus. Virology. 1979;99:49–56. doi: 10.1016/0042-6822(79)90035-7. [DOI] [PubMed] [Google Scholar]
  17. Herrler G., Nagele A., Meier-Ewert H., Bhown A.S., Compans R.W. Isolation and structural analysis of influenza C virion glycoproteins. Virology. 1981;113:439–451. doi: 10.1016/0042-6822(81)90173-2. [DOI] [PubMed] [Google Scholar]
  18. Herrler G., Dürkop I., Becht H., Klenk H.-D. The glycoprotein of influenza C virus is the haemagglutinin, esterase and fusion factor. J. Gen. Virol. 1988;69:839–846. doi: 10.1099/0022-1317-69-4-839. [DOI] [PubMed] [Google Scholar]
  19. Herrler G., Multhaup, Beyreuther K., Klenk H.-D. Serine 71 of the glycoprotein HEF is located at the active site of the acetylesterase of influenza C virus. Arch. Virol. 1988;102:269–274. doi: 10.1007/BF01310831. [DOI] [PubMed] [Google Scholar]
  20. Homma M., Ohyama S., Katagiri S. Age distribution of the antibody to type C influenza virus. Microbiol. Immunol. 1982;26:639–642. doi: 10.1111/mim.1982.26.7.639. [DOI] [PubMed] [Google Scholar]
  21. Jeanloz A. α1-Acid glycoprotein. In: Gottschalk A., editor. Vol. A. Elsevier; Amsterdam: 1972. pp. 565–581. (Glycoproteins). [Google Scholar]
  22. Katagiri S., Ohizumi A., Homma M. An outbreak of type C influenza in a children's home. J. Infect. Dis. 1983;148:51–56. doi: 10.1093/infdis/148.1.51. [DOI] [PubMed] [Google Scholar]
  23. Katagiri S., Ohizumi A., Ohyama S., Homma M. Follow-up study of type C influenza outbreak in a children home. Microbiol. Immunol. 1987;31:337–343. doi: 10.1111/j.1348-0421.1987.tb03094.x. [DOI] [PubMed] [Google Scholar]
  24. Laemmli U.K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970;227:680–685. doi: 10.1038/227680a0. [DOI] [PubMed] [Google Scholar]
  25. Lowry O.H., Rosebrough N.F., Farr A.L., Randall R.J. Protein measurements with the Folin phenol reagent. J. Biol. Chem. 1951;193:265–275. [PubMed] [Google Scholar]
  26. Manuguerra J.C., Dubois C., Hannoun C. Analytical detection of 9(4)-O-acetylated sialoglycoproteins and gangliosides using influenza C virus. Anal. Biochem. 1991;194:425–432. doi: 10.1016/0003-2697(91)90252-O. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Manuguerra J.C., Hannoun C., Aymard M. Demonstration of the occurrence of influenza C virus infection in France. J. Infect. 1991;24:91–99. doi: 10.1016/0163-4453(92)91150-a. [DOI] [PubMed] [Google Scholar]
  28. Miettinen T., Takki-Luukkainen I.T. Use of butyl acetate in determination of sialic acid. Acta Chem. Scand. 1959;13:856–857. [Google Scholar]
  29. Nishimura H., Sugawara K., Kitame F., Nakamura K., Sasaki H. Prevalence of the antibody to influenza C virus in a northern Luzon highland village, Philippines. Microbiol. Immunol. 1987;31:1137–1143. doi: 10.1111/j.1348-0421.1987.tb01348.x. [DOI] [PubMed] [Google Scholar]
  30. Nishimura H., Sugawara K., Kitame F., Nakamura K. Attachment of influenza C virus to human erythrocytes. J. Gen. Virol. 1988;69:2545–2553. doi: 10.1099/0022-1317-69-10-2545. [DOI] [PubMed] [Google Scholar]
  31. O'Callaghan R.J., Labat D.D. Evidence of a soluble substrate for the receptor-destroying enzyme of influenza C virus. Infect. Immunol. 1983;39:305–310. doi: 10.1128/iai.39.1.305-310.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. O'Callaghan R.J., Gohd R.S., Labat D.D. Human antibody to influenza C virus: its age-related distribution and distinction from receptor analogs. Infect. Immunol. 1980;30:500–505. doi: 10.1128/iai.30.2.500-505.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Ohwada K., Kitame F., Homma M. Experimental infections of dogs with type C influenza virus. Microbiol. Immunol. 1986;30:451–460. doi: 10.1111/j.1348-0421.1986.tb02971.x. [DOI] [PubMed] [Google Scholar]
  34. Ravindranaths M.H., Paulson J.C., Irie R.F. Human melanoma antigen O-acetylated ganglioside GD3 is recognized by Cancer antennarius lectin. J. Biol. Chem. 1988;263:2079–2086. [PubMed] [Google Scholar]
  35. Reuter G., Klotz F.W., Howard R.J., Miller L.H., Schauer R. Influence of sialic acid O-acetylation of mouse erythrocyte glycoconjugates on malaria infection. Glycoconjugate J. 1991;8:224–225. [Google Scholar]
  36. Rogers G.N., Herder G., Paulson J.C., Klenk H.-D. Influenza C virus uses 9-O-acetyl-N-neuraminic acid as a high affinity receptor determinant for attachment to cells. J. Biol. Chem. 1986;261:5947–5951. [PubMed] [Google Scholar]
  37. Schauer R. The nature of sialic acids. In: Schauer R., editor. Sialic Acids. Springer; Wien: 1982. pp. 32–33. [Google Scholar]
  38. Schauer R., Reuter G. 1988. Metabolism of O-acetylated sialic acids; pp. 164–165. (Abstr. Proc. German, Symp. Sialic Acids). Berlin. [Google Scholar]
  39. Schauer R., Reuter G., Posadas del Rio F., Herrler G., Klenk H.-D. Isolation and characterization of sialate 9(4)-O-acetylesterase from influenza C virus. Biol. Chem. Hoppe-Seyler. 1988;369:1121–1130. doi: 10.1515/bchm3.1988.369.2.1121. [DOI] [PubMed] [Google Scholar]
  40. Schauer R., Reuter G., Stoll S. Sialate O-acetylesterases: key enzymes in sialic acid metabolism. Biochimie. 1988;70:1511–1519. doi: 10.1016/0300-9084(88)90288-x. [DOI] [PubMed] [Google Scholar]
  41. Svennerholm L. Quantitative estimation of sialic acids. Biochim. Biophys. Acta. 1957;24:604–611. doi: 10.1016/0006-3002(57)90254-8. [DOI] [PubMed] [Google Scholar]
  42. Vlasak R., Muster T., Lauro A., Powers J.C., Palese P. Influenza C virus esterase: analysis of catalytic site, inhibition, and possible function. J. Virol. 1989;63:2056–2062. doi: 10.1128/jvi.63.5.2056-2062.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Warner T.G., O'Brien J.S. Synthesis of 2′-(4-mmethylumbelliferyl)-α-D-N-acetylneuraminic acid and detection of skin fibroblast neuraminidase in normal humans and sialidosis. Biochemistry. 1979;18:2783–2787. doi: 10.1021/bi00580a014. [DOI] [PubMed] [Google Scholar]
  44. Warren L. The thiobarbituric acid assay of sialic acids. J. Biol. Chem. 1959;234:1971–1975. [PubMed] [Google Scholar]
  45. Zimmer G., Reuter G., Schauer R. A new method for detection of 9-O-acetyl-N-acetylneuraminic acid on immobilized glycoconjugates using influenza C virus. Glycoconjugate J. 1991;8:257. [Google Scholar]

Articles from Virus Research are provided here courtesy of Elsevier

RESOURCES