Skip to main content
PMC home page
The EMBO Journal logoLink to The EMBO Journal
. 1992 Feb;11(2):467–472. doi: 10.1002/j.1460-2075.1992.tb05076.x

Expression of factor X and its significance for the determination of paramyxovirus tropism in the chick embryo.

T Ogasawara 1, B Gotoh 1, H Suzuki 1, J Asaka 1, K Shimokata 1, R Rott 1, Y Nagai 1
PMCID: PMC556476  PMID: 1371460

Abstract

Enveloped animal viruses usually possess a surface glycoprotein which mediates fusion between the viral envelope and host cell membrane, hence enabling the initiation of infection, and its biosynthesis often involves post-translational endoproteolytic activation of the inactive precursor by a host cell protease(s). Therefore, the protease distribution in the host must be critical for determining the viral tropism. We previously isolated from chick embryo a cogent candidate endoprotease of this kind for paramyxovirus infection, and demonstrated its identity with factor X (FX), a vitamin K-dependent serine protease in the prothrombin family which, in general, is synthesized in the liver and circulates as one of the plasma proteases essential for blood clotting. Here, we examined FX expression with specific cDNA and antibody probes in a series of embryonic tissues. Many tissues other than the liver expressed the specific mRNA but, in most instances, the translation products remained inactive zymogen forms. The enzymatically active FXa was detectable only in the allantoic fluid and amniotic fluid, and virus spreading was strictly confined to the tissues in direct contact with these FXa-containing fluids. Thus, the ectopically expressed FXa is probably the major host determinant of paramyxovirus tropism in ovo.

Full text

PDF
469

Images in this article

468Image
on p.468
468Image
on p.468
469Image
on p.469

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Adler S., Zett B., Anderson B., Fraley D. S. Effect of volume expansion on renal citrate and ammonia metabolism in KCl-deficient rats. J Clin Invest. 1975 Aug;56(2):391–400. doi: 10.1172/JCI108104. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Akaike T., Molla A., Ando M., Araki S., Maeda H. Molecular mechanism of complex infection by bacteria and virus analyzed by a model using serratial protease and influenza virus in mice. J Virol. 1989 May;63(5):2252–2259. doi: 10.1128/jvi.63.5.2252-2259.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Appleyard G., Davis G. B. Activation of Sendai virus infectivity by an enzyme in chicken amniotic fluid. J Gen Virol. 1983 Apr;64(Pt 4):813–823. doi: 10.1099/0022-1317-64-4-813. [DOI] [PubMed] [Google Scholar]
  4. Blumberg B. M., Giorgi C., Rose K., Kolakofsky D. Sequence determination of the Sendai virus fusion protein gene. J Gen Virol. 1985 Feb;66(Pt 2):317–331. doi: 10.1099/0022-1317-66-2-317. [DOI] [PubMed] [Google Scholar]
  5. Chomczynski P., Sacchi N. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem. 1987 Apr;162(1):156–159. doi: 10.1006/abio.1987.9999. [DOI] [PubMed] [Google Scholar]
  6. Choppin P. W., Scheid A. The role of viral glycoproteins in adsorption, penetration, and pathogenicity of viruses. Rev Infect Dis. 1980 Jan-Feb;2(1):40–61. doi: 10.1093/clinids/2.1.40. [DOI] [PubMed] [Google Scholar]
  7. DeLotto R., Spierer P. A gene required for the specification of dorsal-ventral pattern in Drosophila appears to encode a serine protease. Nature. 1986 Oct 23;323(6090):688–692. doi: 10.1038/323688a0. [DOI] [PubMed] [Google Scholar]
  8. Glickman R. L., Syddall R. J., Iorio R. M., Sheehan J. P., Bratt M. A. Quantitative basic residue requirements in the cleavage-activation site of the fusion glycoprotein as a determinant of virulence for Newcastle disease virus. J Virol. 1988 Jan;62(1):354–356. doi: 10.1128/jvi.62.1.354-356.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Gotoh B., Ogasawara T., Toyoda T., Inocencio N. M., Hamaguchi M., Nagai Y. An endoprotease homologous to the blood clotting factor X as a determinant of viral tropism in chick embryo. EMBO J. 1990 Dec;9(12):4189–4195. doi: 10.1002/j.1460-2075.1990.tb07643.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Grand R. J., Grabham P. W., Gallimore M. J., Gallimore P. H. Modulation of morphological differentiation of human neuroepithelial cells by serine proteases: independence from blood coagulation. EMBO J. 1989 Aug;8(8):2209–2215. doi: 10.1002/j.1460-2075.1989.tb08344.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Hamaguchi M., Grandori C., Hanafusa H. Phosphorylation of cellular proteins in Rous sarcoma virus-infected cells: analysis by use of anti-phosphotyrosine antibodies. Mol Cell Biol. 1988 Aug;8(8):3035–3042. doi: 10.1128/mcb.8.8.3035. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Hidaka Y., Kanda T., Iwasaki K., Nomoto A., Shioda T., Shibuta H. Nucleotide sequence of a Sendai virus genome region covering the entire M gene and the 3' proximal 1013 nucleotides of the F gene. Nucleic Acids Res. 1984 Nov 12;12(21):7965–7973. doi: 10.1093/nar/12.21.7965. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Homma M., Ouchi M. Trypsin action on the growth of Sendai virus in tissue culture cells. 3. Structural difference of Sendai viruses grown in eggs and tissue culture cells. J Virol. 1973 Dec;12(6):1457–1465. doi: 10.1128/jvi.12.6.1457-1465.1973. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Hsu M., Choppin P. W. Analysis of Sendai virus mRNAs with cDNA clones of viral genes and sequences of biologically important regions of the fusion protein. Proc Natl Acad Sci U S A. 1984 Dec;81(24):7732–7736. doi: 10.1073/pnas.81.24.7732. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Kido H., Fukusen N., Katunuma N., Morita T., Iwanaga S. Tryptase from rat mast cells converts bovine prothrombin to thrombin. Biochem Biophys Res Commun. 1985 Oct 30;132(2):613–619. doi: 10.1016/0006-291x(85)91177-5. [DOI] [PubMed] [Google Scholar]
  16. Klenk H. D., Rott R. The molecular biology of influenza virus pathogenicity. Adv Virus Res. 1988;34:247–281. doi: 10.1016/S0065-3527(08)60520-5. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Laemmli U. K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970 Aug 15;227(5259):680–685. doi: 10.1038/227680a0. [DOI] [PubMed] [Google Scholar]
  18. Lazarowitz S. G., Goldberg A. R., Choppin P. W. Proteolytic cleavage by plasmin of the HA polypeptide of influenza virus: host cell activation of serum plasminogen. Virology. 1973 Nov;56(1):172–180. doi: 10.1016/0042-6822(73)90296-1. [DOI] [PubMed] [Google Scholar]
  19. Muramatsu M., Homma M. Trypsin action on the growth of Sendai virus in tissue culture cells. V. An activating enzyme for Sendai virus in the chorioallantoic fluid of the embryonated chicken egg. Microbiol Immunol. 1980;24(2):113–122. doi: 10.1111/j.1348-0421.1980.tb00569.x. [DOI] [PubMed] [Google Scholar]
  20. Nagai Y., Hamaguchi M., Toyoda T. Molecular biology of Newcastle disease virus. Prog Vet Microbiol Immunol. 1989;5:16–64. [PubMed] [Google Scholar]
  21. Nagai Y., Klenk H. D. Activation of precursors to both glycoporteins of Newcastle disease virus by proteolytic cleavage. Virology. 1977 Mar;77(1):125–134. doi: 10.1016/0042-6822(77)90412-3. [DOI] [PubMed] [Google Scholar]
  22. Nagai Y., Klenk H. D., Rott R. Proteolytic cleavage of the viral glycoproteins and its significance for the virulence of Newcastle disease virus. Virology. 1976 Jul 15;72(2):494–508. doi: 10.1016/0042-6822(76)90178-1. [DOI] [PubMed] [Google Scholar]
  23. Nagai Y., Shimokata K., Yoshida T., Hamaguchi M., Iinuma M., Maeno K., Matsumoto T., Klenk H. D., Rott R. The spread of a pathogenic and an apathogenic strain of Newcastle disease virus in the chick embryo as depending on the protease sensitivity of the virus glycoproteins. J Gen Virol. 1979 Nov;45(2):263–272. doi: 10.1099/0022-1317-45-2-263. [DOI] [PubMed] [Google Scholar]
  24. Nishikawa K., Isomura S., Suzuki S., Watanabe E., Hamaguchi M., Yoshida T., Nagai Y. Monoclonal antibodies to the HN glycoprotein of Newcastle disease virus. Biological characterization and use for strain comparisons. Virology. 1983 Oct 30;130(2):318–330. doi: 10.1016/0042-6822(83)90086-7. [DOI] [PubMed] [Google Scholar]
  25. Osterud B., Lindahl U., Seljelid R. Macrophages produce blood coagulation factors. FEBS Lett. 1980 Oct 20;120(1):41–43. doi: 10.1016/0014-5793(80)81041-6. [DOI] [PubMed] [Google Scholar]
  26. Robertson J. S., Bootman J. S., Newman R., Oxford J. S., Daniels R. S., Webster R. G., Schild G. C. Structural changes in the haemagglutinin which accompany egg adaptation of an influenza A(H1N1) virus. Virology. 1987 Sep;160(1):31–37. doi: 10.1016/0042-6822(87)90040-7. [DOI] [PubMed] [Google Scholar]
  27. Rott R., Reinacher M., Orlich M., Klenk H. D. Cleavability of hemagglutinin determines spread of avian influenza viruses in the chorioallantoic membrane of chicken embryo. Arch Virol. 1980;65(2):123–133. doi: 10.1007/BF01317323. [DOI] [PubMed] [Google Scholar]
  28. Scheid A., Choppin P. W. Identification of biological activities of paramyxovirus glycoproteins. Activation of cell fusion, hemolysis, and infectivity of proteolytic cleavage of an inactive precursor protein of Sendai virus. Virology. 1974 Feb;57(2):475–490. doi: 10.1016/0042-6822(74)90187-1. [DOI] [PubMed] [Google Scholar]
  29. Schwartz B. S., Levy G. A., Fair D. S., Edgington T. S. Murine lymphoid procoagulant activity induced by bacterial lipopolysaccharide and immune complexes is a monocyte prothrombinase. J Exp Med. 1982 May 1;155(5):1464–1479. doi: 10.1084/jem.155.5.1464. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Shuman M. A. Thrombin-cellular interactions. Ann N Y Acad Sci. 1986;485:228–239. doi: 10.1111/j.1749-6632.1986.tb34585.x. [DOI] [PubMed] [Google Scholar]
  31. Suzuki H., Harada A., Hayashi Y., Wada K., Asaka J., Gotoh B., Ogasawara T., Nagai Y. Primary structure of the virus activating protease from chick embryo. Its identity with the blood clotting factor Xa. FEBS Lett. 1991 Jun 3;283(2):281–285. doi: 10.1016/0014-5793(91)80608-6. [DOI] [PubMed] [Google Scholar]
  32. Tashiro M., Ciborowski P., Klenk H. D., Pulverer G., Rott R. Role of Staphylococcus protease in the development of influenza pneumonia. Nature. 1987 Feb 5;325(6104):536–537. doi: 10.1038/325536a0. [DOI] [PubMed] [Google Scholar]
  33. Tashiro M., Homma M. Evidence of proteolytic activation of Sendai virus in mouse lung. Arch Virol. 1983;77(2-4):127–137. doi: 10.1007/BF01309262. [DOI] [PubMed] [Google Scholar]
  34. Tashiro M., Homma M. Pneumotropism of Sendai virus in relation to protease-mediated activation in mouse lungs. Infect Immun. 1983 Feb;39(2):879–888. doi: 10.1128/iai.39.2.879-888.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Tashiro M., Yamakawa M., Tobita K., Seto J. T., Klenk H. D., Rott R. Altered budding site of a pantropic mutant of Sendai virus, F1-R, in polarized epithelial cells. J Virol. 1990 Oct;64(10):4672–4677. doi: 10.1128/jvi.64.10.4672-4677.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Toyoda T., Gotoh B., Sakaguchi T., Kida H., Nagai Y. Identification of amino acids relevant to three antigenic determinants on the fusion protein of Newcastle disease virus that are involved in fusion inhibition and neutralization. J Virol. 1988 Nov;62(11):4427–4430. doi: 10.1128/jvi.62.11.4427-4430.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Toyoda T., Sakaguchi T., Hirota H., Gotoh B., Kuma K., Miyata T., Nagai Y. Newcastle disease virus evolution. II. Lack of gene recombination in generating virulent and avirulent strains. Virology. 1989 Apr;169(2):273–282. doi: 10.1016/0042-6822(89)90152-9. [DOI] [PubMed] [Google Scholar]
  38. Toyoda T., Sakaguchi T., Imai K., Inocencio N. M., Gotoh B., Hamaguchi M., Nagai Y. Structural comparison of the cleavage-activation site of the fusion glycoprotein between virulent and avirulent strains of Newcastle disease virus. Virology. 1987 May;158(1):242–247. doi: 10.1016/0042-6822(87)90261-3. [DOI] [PubMed] [Google Scholar]
  39. Webster R. G., Rott R. Influenza virus A pathogenicity: the pivotal role of hemagglutinin. Cell. 1987 Aug 28;50(5):665–666. doi: 10.1016/0092-8674(87)90321-7. [DOI] [PubMed] [Google Scholar]

Articles from The EMBO Journal are provided here courtesy of Nature Publishing Group

RESOURCES