Full text loading...
Research Article
Free
Involvement of the vacuolar H+-ATPase in animal virus entry
- Luis Pérez1 and Luis Carrasco1
- Published: 01 October 1994 https://doi.org/10.1099/0022-1317-75-10-2595
Abstract
Semliki Forest virus (SFV) enters cells by receptor- mediated endocytosis, followed by acidification of endosomes by the action of the vacuolar H+-ATPase. Fusion of the viral and the endosomal membrane delivers the viral genome to the cytoplasm. Direct blockade of the vacuolar H+-ATPase by the selective inhibitor bafilomycin A1 (BFLA1) prevented the infection of cells by SFV, if the compound was present during the first minutes of infection. Attachment and penetration of virus particles were not the targets of the antibiotic. BFLA1 and the ionophore monensin potently blocked SFV infection even at low pH, indicating that acidic pH is not sufficient for SFV to deliver its genome to the cytoplasm, but the proper functioning of the H+- ATPase pump is necessary. Other enveloped RNA- containing viruses, such as vesicular stomatitis virus or influenza virus were also blocked by BFLA1, whereas no effect was observed with Sendai virus, which enters into cells by direct fusion with the plasma membrane. Enveloped DNA-containing viruses, such as herpesviruses and vaccinia virus, infected the cells even when the vacuolar H+-ATPase was inhibited by BFLA1; similar behaviour was observed with poliovirus and adenovirus. Animal virus particles promote the internalization of proteins and other macromolecules during entry. BFLA1 blocked co-entry of the toxin α-sarcin when induced by SFV, but not when induced by Sendai virus. The inhibition of the enzyme responsible for acidification of endosomes by means of the potent inhibitor BFLA1 constitutes a selective and powerful tool to analyse the low-pH dependent mechanism(s) during virus entry and will aid in understanding the mechanisms and routes of entry of animal viruses into cells.
- Received:
- Accepted:
- Published Online:
Article metrics loading...
References
- Almela M. J., Gonzalez M. E., Carrasco L. 1991; Inhibitors of uncoating efficiently block the early permeabilization induced by poliovirus. Journal of Virology 65:2572–2577
- Borsa J., Morash B. D., Sargent M. D., Copps T. P., Lievaart P. A., Szekely J. G. 1979; Two modes of entry of reovirus particles into L cells. Journal of General Virology 45:161–170
- Bowman E. J., Siebers A., Altendorf K. 1988; Bafilomycins: A class of inhibitors of membrane ATPases from microorganisms- animal cells-and plant cells. Proceedings of the National Academy of Sciences U.S.A.: 857972–7976
- Brown D. T., Burlingham B. T. 1973; Penetration of host cell membranes by adenovirus 2. Journal of Virology 12:386–396
- Carrasco L. 1981; Modification of membrane permeability induced by animal viruses early in infection. Virology 113:623–629
- Carrasco L., Esteban M. 1982; Modification of membrane permeability in vaccinia virus-infected cells. Virology 117:62–69
- Carrasco L., Otero M. J., Castrillo J. L. 1989; Modification of membrane permeability by animal viruses. Pharmacological Therapeutics 40:171–212
- Carrasco L., Perez L., Irurzun A., Lama J., Martinez-Abarca F. , Guinea R., Castrillo J. L., Sanz M. A., Ayala M. J. 1993; Modification of membrane permeability by animal viruses. In Regulation of Gene Expression in Animal Viruses pp 283–305 Carrasco L., Sonenberg N., Wimmer E. Edited by New York: Plenum Press;
- Cassell S., Edwards J., Brown D. T. 1984; Effect of lysosomotropic weak bases on infection of BHK-21 cells by Sindbis virus. Journal of Virology 52:857–864
- Compans R. C., Holmes K. V., Dales S., Choppin P. W. 1964; An electron microscopic study of moderate and virulent virus-cell interactions of the parainfluenza virus SV5. Virology 30:411–426
- Coombs K., Mann E., Edwards J., Brown D. T. 1981; Effects of chloroquine and cytochalasin B on the infection of cells by Sindbis virus and Vesicular Stomatitis virus. Journal of Virology 37:1060–1065
- Cotten M., Wagner E., Zatloukal K., Phillips S., Curiel D. T., Birnstiel M. L. 1992; High-efficiency receptor-mediated delivery of small and large (48 kilobase gene constructs using the endosome-disruption activity of defective or chemically inactivated adenovirus particles. Proceedings of the National Academy of Sciences U.S.A.: 896094–6098
- Dales S. 1973; Early events in cell-animal virus interactions. Bacteriological Reviews 37:103–135
- Dimmock N. J. 1982; Review article initial stages in infection with animal viruses. Journal of General Virology 59:1–22
- Doms R. W., Blumenthal R., Moss B. 1990; Fusion of intra- and extracellular forms of vaccinia virus with the cell membrane. Journal of Virology 64:4884–4892
- Dunnebacke T. H., Levinthal J. D., Williams R. C. 1969; Entry and release of poliovirus as observed by electron microscopy of cultured cells. Journal of Virology 4:505–513
- Edwards J., Brown D. T. 1991; Sindbis virus infection of a Chinese hamster ovary cell mutant defective in the acidification of endosomes. Virology 182:28–33
- Edwards J., Mann E., Brown D. T. 1983; Conformational changes in Sindbis virus envelope proteins accompanying exposure to low pH. Journal of Virology 45:1090–1097
- Fernández-Puentes C., Carrasco L. 1980; Viral infection permeabilizes mammalian cells to protein toxins. Cell 20:769–775
- FitzGerald D. J., Padmanabhan R., Pastan I., Willingham M. C. 1983; Adenovirus-induced release of epidermal growth factor and pseudomonas toxin into the cytosol of KB cells during receptor- mediated endocytosis. Cell 32:607–617
- Flynn D. C., Meyer W. J., Mackenzie J. M. J., Johnston R. E. 1990; A conformational change in Sindbis virus glycoproteins El and E2 is detected at the plasma membrane as a consequence of early virus-cell interaction. Journal of Virology 64:3643–3653
- Fuller A. O., Lee W.-C. 1992; Herpes simplex virus type 1 entry through a cascade of virus-cell interactions requires different roles of gD and gH in penetration. Journal of Virology 66:5002–5012
- González M. E., Carrasco L. 1987; Animal viruses promote the entry of polysaccharides with antiviral activity into cells. Biochemical and Biophysical Research Communications 146:1303–1310
- Gromeier M., Wetz K. 1990; Kinetics of poliovirus uncoating in HeLa cells in a nonacidic environment. Journal of Virology 64:3590–3597
- Haywood A. M. 1994; Virus receptors: binding, adhesion strengthening, and changes in viral structure. Journal of Virology 68:1–5
- Helenius A., Marsh M., White J. 1982; Inhibition of Semliki forest virus penetration by lysosomotropic weak bases. Journal of General Virology 58:47–61
- Helenius A., Kielian M., Wellsteed J., Mellman I., Rudnick G. . 1985; Effects of monovalent cations on Semliki Forest virus entry into BHK-21 cells. Journal of Biological Chemistry 260:5691–5697
- Hoekstra D., Kok J. W. 1989; Entry mechanisms of enveloped viruses. Implications for fusion of intracellular membranes. Bioscience Reports 9:273–305
- Kaljot K. T., Shaw R. D., Rubin D. H., Greenberg H. B. 1988; Infectious rotavirus enters cells by direct cell membrane penetration, not by endocytosis. Journal of Virology 62:1136–1144
- Kielian M., Helenius A. 1985; pH-induced alterations in the fusogenic spike protein of Semliki Forest virus. Journal of Cell Biology 101:2284–2291
- Lamb R. A. 1993; Paramyxovirus fusion: a hypothesis for changes. Virology 197:1–11
- Madshus I. H., Olsnes S., Sandvig K. 1984a; Requirements for entry of poliovirus RNA into cells at low pH. EMBO Journal 3:1945–1950
- Madshus I. H., Olsnes S., Sandvig K. 1984b; Mechanism of entry into the cytosol of poliovirus type 1: requirement for low pH. Journal of Cell Biology 98:1194–1200
- Marsh M., Helenius A. 1989; Virus entry into animal cells. Advances in Virus Research 36:107–151
- Maxfield F. R. 1982; Weak bases and ionophores rapidly and reversibly raise the pH of endocytic vesicles in cultured mouse fibroblasts. Journal of Cell Biology 95:676–681
- Mellman I., Fuchs R., Helenius A. 1986; Acidification of the endocytic and exocytic pathways. Annual Review of Biochemistry 55:663–700
- Meyer W. J., Gidwitz S., Ayers V. K., Schoepp R. J., Johnston R. E. 1992; Conformational alteration of Sindbis virion glycoproteins induced by heat, reducing agents, or low pH. Journal of Virology 66:3504–3513
- Miller D. K., Lenard J. 1981; Antihistaminics, local anesthetics, and other amines as antiviral agents. Proceedings of the National Academy of Sciences U.S.A.: 783605–3609
- Morrison T., Portner A. 1991 The Paramyxoviruses Kingsbury D. W. Edited by New York: Plenum Press;
- Nelson N., Taiz L. 1989; The evolution of H+-ATPases. Trends in Biochemical Sciences 14:113–116
- Otero M. J., Carrasco L. 1987; Proteins are cointemalized with virion particles during early infection. Virology 160:75–80
- Perez L., Carrasco L. 1993; Entry of poliovirus into cells does not require a low-pH step. Journal of Virology 67:4543–4548
- Schneider D. L. 1987; The proton pump ATPase of lysosomes and related organelles of the vacuolar apparatus. Biochimica et Biophysica Acta 895:1–10
- Seglen P. O. 1983; Inhibitors of lysosomal function. Methods in Enzymology 96:737–764
- Skehel J. J., Hay A. J., Armstrong J. A. 1978; On the mechanism of inhibition of influenza virus replication by amantadine hydrochloride. Journal of General Virology 38:97–110
- Stegmann T., Doms R. W., Helenius A. 1989; Protein-mediated membrane fusion. Annual Review of Biophysics and Biophysical Chemistry 18:187–211
- Sturzenbecker L. J., Nibert M., Furlong D., Fields B. N. 1987; Intracellular digestion of reovirus particles requires a low pH and is an essential step in the viral infectious cycle. Journal of Virology 61:2351–2361
- Svensson U., Persson R. 1984; Entry of adenovirus 2 into HeLa cells. Journal of Virology 51:687–694
- Svensson U. 1985; Role of vesicles during adenovirus 2 internalization into HeLa cells. Journal of Virology 55:442–449
- Varga M. J., Weibull C., Everitt E. 1991; Infectious entry pathway of adenovirus type 2. Journal of Virology 65:6061–6070
- Wagner E., Zatloukal K., Cotten M., Kirlappos H., Mechtler K., Curiel D. T., Birnstiel M. L. 1992; Coupling of aedeno- virus to transferrin-polylysine/DNA complexes greatly enhances receptor-mediated gene delivery and expression of transfected genes. Proceedings of the National Academy of Sciences U.S.A.: 896099–6103
- White J., Kartenbeck J., Helenius A. 1980; Fusion of Semliki forest virus with the plasma membrane can be induced by low pH. Journal of Cell Biology 87:264–272
- White J. M. 1990; Viral and cellular membrane fusion proteins. Annual Review of Physiology 52:675–697
- Wileman T., Harding C., Stahl P. 1985; Receptor-mediated endocytosis. Biochemical Journal 232:1–14
- Wittels M., Spear P. G. 1991; Penetration of cells by herpes simplex virus does not require a low pH-dependent endocytic pathway. Virus Research 18:271–290
- Yoshimori T., Yamamoto A., Moriyama Y., Futai M., Tashiro Y. 1991; Bafilomycin Al, a specific inhibitor of vacuolar-type H(+)-ATPase, inhibits acidification and protein degradation in lysosomes of cultured cells. Journal of Biological Chemistry 266:17707–17712
- Zeuzem S., Feick P., Zimmermann P., Haase W., Kahn R. A., Schulz I. 1992; Intravesicular acidification correlates with binding of ADP-ribosylation factor to microsomal membranes. Proceedings of the National Academy of Sciences U.S.A.: 896619–6623
Data & Media loading...