Abstracts
Prostaglandin A1 (PGA1) inhibits Mayaro virus replication in Aedes albopictus cells at nontoxic doses to uninfected cells. At 10 µg/ml, PGA1 decreases virus production by 90%. The presence of PGA1 during virus adsorption, with no treatment after infection, reduces virus yield by 41%. Antiviral activity is observed even when treatment starts at one or two hours post-infection. However, in cells pre-treated with PGA1 during 24 hours, virus replication is not impaired. Thus, events ocurring during initial stages of infection and after virus adsorption and penetration must be the target of PGA1 action. SDS-PAGE analysis of 35S-methionine labelled proteins shows that PGA1 inhibits the synthesis of viral proteins and induces the synthesis of polypeptides with molecular weight of 70 kDa, 57 kDa and 23 kDa. In cells pre-treated with actinomycin D the induction of those proteins is suppressed. In addition, actinomycin D treatment prevents PGA1antiviral activity, indicating that PGA1-induced stress proteins are probably involved in this mechanism.
Mayaro virus; Prostaglandin; Aedes albopictus cells; Heat-shock proteins; Actinomycin D
Prostaglandin A1 (PGA1) inibe a replicação do vírus Mayaro em células de Aedes albopictus em doses não tóxicas para células não infectadas. A presença de PGA1 durante o período de adsorção, reduz a produção do vírus em 41%. A atividade antiviral é observada mesmo quando o tratamento é iniciado com 1 ou 2 horas após a infecção. Entretanto, em células pré-tratadas com PGA1 durante 24 h a replicação viral é inalterada. A análise das proteínas marcadas com 35S-metionina, por eletroforese em gel de poliacrilamida, mostra que a PGA1 inibe a síntese de proteínas virais e induz a síntese de polipeptídeos com peso molecular de 70 Kda, 57 Kda e 23 Kda. Em células pré-tratadas com actinomicina D observa-se um bloqueio da atividade antiviral, indicando que as proteínas de estresse induzidas pela PGA1 estão envolvidas neste mecanismo.
Vírus Mayaro; Prostaglandina A1; Células de Aedes albopictus; Proteínas de Choque Térmico; Actinomicina D
INHIBITION OF MAYARO VIRUS REPLICATION BY PROSTAGLANDIN A1 IN AEDES ALBOPICTUS CELLS
Joel Antonio Barbosa1 and Moacyr Alcoforado Rebello2** Corresponding author. Mailing address: Departamento de Virologia, Instituto de Microbiologia Prof. Paulo de Góes, Universidade Federal do Rio de Janeiro, CEP 21941-590, Rio de Janeiro, RJ, Brasil. Telefax: (+5521) 270-8344 / 270-8793
Instituto de Biofísica Carlos Chagas Filho1 and Departamento de Virologia do Instituto de Microbiologia Prof. Paulo de Góes2, Universidade Federal do Rio de Janeiro, Rio de Janeiro, RJ, Brasil.
Approved: July 23, 1998
ABSTRACT
Prostaglandin A1 (PGA1) inhibits Mayaro virus replication in Aedes albopictus cells at nontoxic doses to uninfected cells. At 10 µg/ml, PGA1 decreases virus production by 90%. The presence of PGA1 during virus adsorption, with no treatment after infection, reduces virus yield by 41%. Antiviral activity is observed even when treatment starts at one or two hours post-infection. However, in cells pre-treated with PGA1 during 24 hours, virus replication is not impaired. Thus, events ocurring during initial stages of infection and after virus adsorption and penetration must be the target of PGA1 action. SDS-PAGE analysis of 35S-methionine labelled proteins shows that PGA1 inhibits the synthesis of viral proteins and induces the synthesis of polypeptides with molecular weight of 70 kDa, 57 kDa and 23 kDa. In cells pre-treated with actinomycin D the induction of those proteins is suppressed. In addition, actinomycin D treatment prevents PGA1 antiviral activity, indicating that PGA1-induced stress proteins are probably involved in this mechanism.
Key words: Mayaro virus; Prostaglandin; Aedes albopictus cells; Heat-shock proteins; Actinomycin D
Prostaglandins of the A and J type, characterized by the presence of an a, b unsaturated carbonyl group in the cyclopentane ring, have been shown to inhibit the replication of several DNA and RNA virus. However, the antiviral mechanism is not yet well understood and contrasting results have been reported for different virus-cell systems (31).
Several PGs were found to induce heat shock proteins (29, 31). PGA
12Mayaro virus (Alphavirus genus, Togaviridae family) is an arthropod-borne virus antigenically related to Semliki Forest Virus (8). Mayaro virus, like other Togaviridae, is perpetuated in nature by its ability to infect and replicate both in vertebrate and invertebrate cells (6). In Brazil, this virus has been isolated from human and other mammalian species in the Amazon region. Clinical manifestations of human infection were described as a feverish illness, followed by headache, epigastric pain, backache, chills, nausea and photophobia (8, 3, 9).
We have been studying the Mayaro virus replication in mammalian cells and in mosquito (Aedes albopictus) cells (15, 16). The replication of Mayaro virus in Vero cells is concomitant with an inhibition of host macromolecular synthesis and cythopatic effects. In contrast infection of Aedes albopictus cells with Mayaro virus is characterized by a persistent infection.
Prostaglandins and other active derivatives of polyunsaturated fatty acids have been detected in a large number of invertebrate species (33, 34). Recently, Petzel et al. (21) described the presence of arachidonic acid and prostaglandin E
Aedes aegypti.We found recently that in PGA
1Aedes albopictusAedes albopictus1Aedes albopictusIn the present paper we studied the effect PGA
1Aedes albopictus1Cells and virusAedes albopictus cells, clone C6/36, were used in this study (12). This cell line was a gift from Dr. R.E. Shope, Arbovirus Unit, Yale University, New Haven, CT, USA. The cells were grown in 60cm
2o37oProstaglandin A
1oVirus infection
Aedes albopictus cells were infected with 1 or 5 PFU per cell in medium without serum. After 60 minutes at 28
oo2Virus titrations were performed by plaque assay in Vero cells (25). Briefly, virus dilutions (0.5 ml) were added to cell monolayers (60 mm diameter Petri dishes) that had just reached confluency. After 60 min at 37
o2oAnalysis of [35S]methionine labelled proteins by polyacrylamide gel electrophoresisProteins were labelled with [35S]methionine (20 µCi/ml) and monolayers were directly resuspended in 70 µl of loading buffer (62.5 mM Tris-HCl, pH 6.8; 2% SDS; 10% glycerol; 5% 2-mercaptoethanol and 0.001% bromophenol blue). Samples were then heated for 5 min at 95oC and subjected to electrophoresis on one-dimensional 12.5% polyacrylamide gels, using the SDS buffer system of Laemmli (13) at room temperature. The dried gels were exposed to Kodak X-Omat (YAR-S) film. The molecular mass of proteins was determined by co-electrophoresis of standard proteins (Pharmacia). Molecular masses in KDa are indicated to the right (viral proteins) or to the left (cellular proteins) of the gel.
RESULTS
Effect of PGA1 on Mayaro virus replication
Confluent monolayers of A. albopictus cells were infected with Mayaro virus (1 PFU/cell), and treated with different concentrations of PGA1from 1h after infection onwards. Supernatants were collected 24h p.i. and virus titers (triplicate samples) were determined by plaque assay. Fig. 1 shows that PGA1 inhibits virus replication in a dose-dependent manner, with concentrations of 1.0µg/ml being able to reduce virus yield by 50% and doses between 7.5 and 10 µg/ml being effective in causing a 90-95% inhibition of virus production. The concentration of 10µg/ml was found to be the most active nontoxic dose, not having altered cell viability in uninfected cells and was used in all the following experiments. The effect of PGA1 treatment during virus adsorption was then studied. Cells were infected with Mayaro virus suspension containing PGA1 (10 µg/ml) or control diluent. After 1h adsortion at 28oC, virus inocula were removed and the monolayers were washed three times with PBS to remove PGA1. Growth medium was added and cells were incubated for 24h. The presence of PGA1 during virus adsorption was found to decrease the number of virus plaques by 41 % (Table 1 protocol A). The antiviral action of PGA1 was observed even when the treatment started 1 or 2h p.i. (Table 1 protocol B and C). However, in cells pre-treated with PGA1during 24h (with no treatment after infection) virus replication was not impaired (protocols D and E).
- Effect of PGA1 on Mayaro virus production. Dose-dependent inhibition. A. albopictus cells were infected with Mayaro virus (1 pfu/ml) and treated with different concentrations of PGA1. Virus production was determined (triplicate samples) 24 hours post-infection as described in Materials and Methods.
- Inhibition of Mayaro virus in A. albopictus cells by PGA1 treatment. Virus yield of controls was 6,7 x 107 PFU/ml.
Cells were infected with Mayaro virus (1 PFU/cell) and treated with PGA1 (10 µg/ml). Virus yields were collected 24 hours post-infection and titrated (triplicate samples) as described in Material and Methods.
Protocol A: PGA1 treatment only during virus adsorption period. Protocol B : PGA1 treatment started 1 hour after virus adsorption period. Protocol C: PGA1 treatment started 2 hours after virus adsorption period. Protocol D : Cells were pre-treated with PGA1 during 24 hours. After this period, monolayers were washed with PBS, infected with Mayaro virus and incubated with growth medium in the presence of PGA1. Twenty four hours later, the virus were titrated. Protocol E : Cells were pre-treated with PGA1 during 24 hours. After this period, monolayers were washed with PBS, infected with Mayaro virus and incubated in growth medium. Twenty four hours later, the virus were titrated.
Effect of PGA1 on protein synthesis
Previous results from our laboratory (Mezencio and Rebello, 1993) showed that in Mayaro virus infected BHK-21 cells and in A. albopictus cells, six viral proteins could be detected. Three of them are structural proteins (molecular weight of 54kDa, 50 kDa and 34 kDa,) and the other three are precursors of viral proteins (molecular weight of 110 kDa, 64kDa and 62kDa).
To examine the effect of PGA1 on the protein synthesis of Mayaro virus infected A. albopictus cells, confluent monolayers were infected (5 PFU/ml) and 1h later, virus inocula were removed and culture medium containing PGA1 or control diluent was added. After 24h, the medium was supplemented with 20 µCi/ml of 35S-methionine. One hour later, the medium was removed and the proteins were analyzed by SDS-polyacrylamide gel electrophoresis. As shown in Fig. 2, treatment with PGA1 suppressed viral protein synthesis. The synthesis of protein p34 was dramatically reduced in cells treated with PGA1 (lanes C and D) and the synthesis of the two precursors (p64 and p62) was also modified (lane D). We also observed that in mock infected cells, the presence of PGA1 stimulated the synthesis of three polypeptides (stress proteins) with molecular weights of 70kDa, 57kDa and 23kDa (lane B).
- Effect of PGA1 on Mayaro virus infected cells. A. albopictus cells were infected (lanes C and D) with Mayaro virus (5 pfu/ml) or mock infected (lanes A and B) and maintained in growth medium for 24 hours in the presence of PGA1 (lanes B and D). After this period, the cells were labelled with 35S-methionine (20 µCi/ml) for 1 hour and cellular extracts were subjected to polyacrylamide gel electrophoresis.
Effect of Actinomycin D (AMD) and PGA1 on synthesis of Mayaro virus protein
In Fig. 3 we show that, in cells treated with AMD (2 µg/ml) the induction of stress proteins was suppressed (lane B). In A. albopictus infected cells, we observed that in the presence of AMD there was only a partial reduction on viral protein synthesis, probably as a consequence of the long treatment with this drug (lane D). In cells treated with PGA
11- Effect of PGA1 and actinomycin D in Mayaro virus protein synthesis. A albopictus cells were infected (lanes C, D, E and F) with Mayaro virus (5pfu/ml) or mock infected (lanes A and B) and maintained in growth medium for 24 hours, in the presence of PGA1 (lanes A, B, E and F) and actinomycin D (lanes B, D and F). After this period the cells were labeled with 35S-methionine (20 µCi/ml) for 1 hour and cellular extracts were subjected to polyacrylamide gel electrophoresis.
The presence of PGA
11et al.The pre-treatment of A. albopictus cells with PGA
1et al.1The examination of viral proteins revealed that PGA
1et al.10et al.2Recent results from experiments concerning the effects of PGJ
23Actinomycin D blocked the PGA
111o11On the other hand, Parker et al. (20) observed that in mouse L929 cells actinomycin D inhibited cellular RNA synthesis but failed to block the antiviral activity of PGA
1The results presented in this paper show that in cultured A. albopictus cells, PGA
1et al.et al.RESUMO
Inibição da replicação do vírus Mayaro pela prostaglandin A1 em células de Aedes albopictus
Prostaglandin A1 (PGA1) inibe a replicação do vírus Mayaro em células de Aedes albopictus em doses não tóxicas para células não infectadas. A presença de PGA1 durante o período de adsorção, reduz a produção do vírus em 41%. A atividade antiviral é observada mesmo quando o tratamento é iniciado com 1 ou 2 horas após a infecção. Entretanto, em células pré-tratadas com PGA1 durante 24 h a replicação viral é inalterada. A análise das proteínas marcadas com 35S-metionina, por eletroforese em gel de poliacrilamida, mostra que a PGA1 inibe a síntese de proteínas virais e induz a síntese de polipeptídeos com peso molecular de 70 Kda, 57 Kda e 23 Kda. Em células pré-tratadas com actinomicina D observa-se um bloqueio da atividade antiviral, indicando que as proteínas de estresse induzidas pela PGA1 estão envolvidas neste mecanismo.
Palavras-chave: Vírus Mayaro; Prostaglandina A1; Células de Aedes albopictus; Proteínas de Choque Térmico, Actinomicina D.
REFERENCES
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21. Petzel, D.H., Parrish, A.K., Ogg, C.L., Witters, N.A., Howard, R.W. and Stanley-Samuelson, D.W. Arachidonic acid and prostaglandin E2 in Malpighian tubules of female yellow fever mosquitos. Insect Biochem. Molec. Biol., 23:431-437, 1993.
22. Pica, F., De Marco, A., De Cesare, F. and Santoro, M.G. Inhibition of vesicular stomatitis virus replication by 12 - prostaglandin J2 is regulated at two separate levels and is associated with induction of stress proteins synthesis. Antiviral Res., 20:193-208, 1993.
23. Pottathil, R., Chandrabose, K.A., Cuatrecasas, P. and Lang, D.J. Establishment of the interferon-mediated antiviral state : Role of fatty acid cyclooxygenase. Proc. Natl. Acad. Sci., 77:5437-5440, 1980.
24. Rabindran, S.K., Giorgi, G., Clos, J., and Wu, C. Molecular cloning and expression of a human heat shock factor HSF1. Proc. Natl. Acad. Sci., 88:6906-6910, 1991.
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29. Santoro, M.G., Garaci, E., and Amici, C. Prostaglandin with antiproliferative activity induce the synthesis of a heat shock protein in human cells. Proc. Natl. Acad. Sci., USA, 86:8407-8411, 1989a.
30. Santoro, M.G., Amici, C., Elia, G., Benedetto, A., and Garaci, E. Inhibition of virus protein glycosylation as the mechanism of the antiviral action of prostaglandin A in Sendai virus-infected cells. J. Gen. Virol., 70:789-900, 1989b.
31. Santoro, M.G., Garaci, E. and Amici, C. Induction of HSP70 by prostaglandins. In : M.J. Schlesinger, M.G. Santoro, E. Garaci (Eds.). Stress proteins : Induction and function. Springer-Verlag, Berlin, 1990.
32. Stanley-Samuelson, D.W., Jensen, E., Nickerson, K.W., Tiebel, K., Ogg, C.L., and Howard, R.W. Insect immune response to bacterial infection is mediated by eicosanoids. Proc. Natl. Acad. Sci., 88:1064-1068, 1991.
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-
1Amici, C., Palamara, A.T., Garaci, E. and Santoro, M.G. Inhibition of Sendai virus replication by 12 prostaglandin J.2: induction of heat shock protein synthesis and alteration of protein glycosylation. Antiviral Res, 19:128-134, 1992.
-
2Amici, C., Giorgi, C., Rossi, A. and Santoro, M.G. Selective inhibition of virus protein synthesis by prostaglandin A1 : a translation block associated with HSP70 synthesis. J. Virol, 68:6890-6899, 1994.
-
3Anderson, C.R., Downs, W.G., Wattley, G.M., Alin, N.W., and Reeser, A.A. Mayaro virus : a new human disease agent II. Isolation from blood of patients in Trinidad. Am. J. Trop. Med. Hyg, 6:1012-1016, 1957.
-
4Ankel, H., Mittnacht, S. and Jacobsen, H. Antiviral activity of Prostaglandin A on encephalomyocarditis virus infected cells : A unique effect unrelated to interferon. J. Gen. Virol, 66:2355-2364, 1985.
-
5Barbosa, J.A. and Rebello, M.A. Prostaglandin A1 inhibits replication of Mayaro virus in Aedes albopictus cells. Braz. J. Med. Biol. Res, 28:27-30, 1995.
-
6Brown, D.T. and Condreay, L.D. Replication of Alphavirus in mosquito cells. In : Schlesinger S. & Schlesinger M.J. (Editors), The Togaviridae and Flaviridae. Plenum Press, New York, 171-207, 1986.
-
7Carvalho, M.G.C. and Rebello, M.A. Induction of heat shock proteins during the growth of Aedes albopictus cells. Insect Biochemistry, 17:199-206, 1987.
-
8Casals, J. and Whitman, L. Mayaro virus : a new human disease agent. I. relationship to other arboviruses. Am. J. Trop. Med. and Hyg, 6:1004-1011, 1957.
-
9Causey, O.R. and Maroja, O.M. Mayaro virus : a new human disease agent. III Investigation of an epidemic of acute Febrile illness on the River Guama in Para, Brazilian isolation of Mayaro virus as a causative agent. Am. J. Trop. Med. Hyg, 6:1017-1023, 1957.
-
10Fitzpatrick, F.A., and Stringfellow, D.A. Virus and interferon effects on cellular prostaglandins biosynthesis. J. Immunol., 125:431-437, 1980.
-
11Goodwin, J.S. and Webb, D.R. Regulation of the immune response by prostaglandins. Clin. Immunol. Immunopathol., 15:106-122, 1980.
-
12Igarashi, A. Isolation of a Singh’s Aedes albopictus cell clone sensitive to dengue and chikungunya viruses. J. Gen. Virol, 40:531-544, 1978.
-
13Laemmli, U.K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature, 277:680-685. 1970.
-
14Mastromarino, P., Conti, C., Petruzziello, R., De Marco, A., Pica, F. and Santoro, M.G. Inhibition of Sindbis virus replication by cyclopentenone prostaglandins : a cell-mediated event associated with heat shock protein synthesis. Antiviral Res, 20:209-222, 1993.
-
15Mezencio, J.M.S., de Souza, W., Fonseca, M.E.F. and Rebello, M.A. Replication of Mayaro virus in Aedes albopictus cells : an electron microscopic study. Arch. Virol, 104:299-308, 1989.
-
16Mezencio, J.M.S., de Souza, M., Fonseca, M.E.F. and Rebello, M.A. Ultrastructural study of Mayaro virus replication in BHK-21 cells. Arch. Virol, 114:229-235, 1990.
-
17Mezencio, J.M.S. and Rebello, M.A. Mayaro virus proteins. Mem. Inst. Oswaldo Cruz, 88:299-304, 1993.
-
18Miller, J.S., Nguyen, T., and Stanley-Samuelson, D.W. Eicosanoids mediate insect modulation response to bacterial infections. Proc. Natl. Acad. Sci, 91:12418-12422, 1994.
-
19Ohno, K., Fukushima, M., Fujiwara, F., and Narumiya, S. Induction o 68,000 dalton heat shock proteins by cyclopentenone prostaglandins. J. Biol Chem, 263:19764-19770, 1988.
-
20Parker, J., Ahrens, P.B. and Ankel, H. Antiviral effect of cyclopentenone prostaglandins on vesicular stomatitis virus replication. Antiviral Res, 26:83-96, 1995.
-
21Petzel, D.H., Parrish, A.K., Ogg, C.L., Witters, N.A., Howard, R.W. and Stanley-Samuelson, D.W. Arachidonic acid and prostaglandin E2 in Malpighian tubules of female yellow fever mosquitos. Insect Biochem. Molec. Biol, 23:431-437, 1993.
-
22Pica, F., De Marco, A., De Cesare, F. and Santoro, M.G. Inhibition of vesicular stomatitis virus replication by 12 - prostaglandin J2 is regulated at two separate levels and is associated with induction of stress proteins synthesis. Antiviral Res, 20:193-208, 1993.
-
23Pottathil, R., Chandrabose, K.A., Cuatrecasas, P. and Lang, D.J. Establishment of the interferon-mediated antiviral state : Role of fatty acid cyclooxygenase. Proc. Natl. Acad. Sci, 77:5437-5440, 1980.
-
24Rabindran, S.K., Giorgi, G., Clos, J., and Wu, C. Molecular cloning and expression of a human heat shock factor HSF1. Proc. Natl. Acad. Sci, 88:6906-6910, 1991.
-
25Rebello, M.C.S., Fonseca, M.E.F., Marinho, J.O. and Rebello, M.A. Interferon action on Mayaro virus replication. Acta Virol, 37:223-231, 1993.
-
26Samuelsson, B. Prostaglandins, tromboxanes, and leukotrienes : biochemical pathways. In : Powles T.J., Bochman R.S., Honn K.V., Ramwell P. (Eds.). Prostaglandins and cancer First International Conference. Alan R. Liss. Inc., New York, 1982, pp 1-19.
-
27Santoro, M.G., Jaffe,B.M., and Esteban, M. Prostaglandin A inhibits the replication of vesicular stomatitis virus: Effect on virus glycoprotein. J. Gen. Virol, 64:2797-2801, 1983.
-
28Santoro, M.G. Involvement of proteins synthesis in the antiproliferative and the antiviral action of prostaglandins. In : Garaci E., Paoletti R., Santoro M.G. (eds.) Prostaglandins in cancer research Springer, Berlin, Heidelberger, New York, Tokyo, 1987, pp. 97-114.
-
29Santoro, M.G., Garaci, E., and Amici, C. Prostaglandin with antiproliferative activity induce the synthesis of a heat shock protein in human cells. Proc. Natl. Acad. Sci, USA, 86:8407-8411, 1989a.
-
30Santoro, M.G., Amici, C., Elia, G., Benedetto, A., and Garaci, E. Inhibition of virus protein glycosylation as the mechanism of the antiviral action of prostaglandin A in Sendai virus-infected cells. J. Gen. Virol, 70:789-900, 1989b.
-
31Santoro, M.G., Garaci, E. and Amici, C. Induction of HSP70 by prostaglandins. In : M.J. Schlesinger, M.G. Santoro, E. Garaci (Eds.). Stress proteins : Induction and function Springer-Verlag, Berlin, 1990.
-
32Stanley-Samuelson, D.W., Jensen, E., Nickerson, K.W., Tiebel, K., Ogg, C.L., and Howard, R.W. Insect immune response to bacterial infection is mediated by eicosanoids. Proc. Natl. Acad. Sci, 88:1064-1068, 1991.
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Publication Dates
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Publication in this collection
26 Feb 1999 -
Date of issue
Sept 1998
History
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Accepted
23 July 1998 -
Reviewed
17 Apr 1998 -
Received
09 Feb 1998