The Prevention of Early Vaccinia-virus-induced Cytopathic Effects by Inhibition of Protein Synthesis

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1 J. gen. ViroL (1968), 3, Printed in Great Britain 5I The Prevention of Early Vaccinia-virus-induced Cytopathic Effects by Inhibition of Protein Synthesis By R. BABLANIAN Department of Microbiology and Immunology, State University of New York, Downstate Medical Center, Brooklyn, N.Y. I 1203 (Accepted I5 January I968) SUMMARY Infection of LLC-MK 2 cells with the International Health Division strain of vaccinia vh'us caused rounding of all cells within 2 to 3 hr after infection. Puromycin, at a concentration of 330 #g.ml., completely prevented the early virus-induced cytopathological changes as well as virus multiplication; however, at 33 #g.ml. the compound did not prevent the cytopathic effects of vaccinia virus, in spite of the fact that virus multiplication was largely inhibited. Treatment of cells for 4 hr with puromycin at 33ozg.ml. did not alter the rate of cell division when the compound was removed. When the antibiotic (33ozg.ml.) was removed from infected cultures after a treatment period of 4 hr, virus-induced cell damage began almost immediately after removal and by I hr all cells were rounded. Actinomycin D, 5zg.ml., also protected the cells from the early vacciniavirus-induced cytopathic effects. At o'5*g.ml., although growth of virus was inhibited, no protection against viral cytopathic effects was observed. In LLC-MK x cells virus-induced morphological damage was not prevented by p-fluorophenylalanine, 5-fluoro-e'-deoxyuridine, and isatin-fithiosemicarbazone--compounds known to inhibit the reproduction of vaccinia virus. Ultraviolet-irradiated virus, which had lost its infectivity, was still capable of causing early cell damage. These findings suggest that the early virus-induced cytopathological effects, previously considered the' toxic' effects of the virus, are brought about by the synthesis of virus-induced protein(s). INTRODUCTION Poxviruses are known to cause cytopathological changes in a number of cell types in the complete absence of production of infectious virus or before the production of such virus (Bernkopf, Nishmi & Rosin, 1959; Brown, Mayyasi & Officer, 1959; Hanafusa, 196o; Appleyard, Westwood & Zwartouw, I962). This virus-induced morphological damage has been thought of as a 'toxic' effect of the virus (Brown et al 1959). It occurs in the presence of inhibitors of virus reproduction such as sodium azide (Brown et al. 1959; Easterbrook, i96i; Appleyard et al. I962), and isatin-flthiosemicarbazone (Appleyard, Hume & Westwood, 1965). Evidence has been reported that the early 'toxic' effect of the virus is associated with the virus particle itself (Brown et al. 1959; Hanafusa, 196o). The cell rounding or' toxic' effect has been interpreted as a cellular response to the ingestion of virus particles for which no information encoded in the viral genome is required (Joklik, 1966 ). 4-2

2 5 2 R. BABLANIAN Bablanian, Eggers & Tamm (1965 b) reported that poliovirus-induced cell damage is linked to the synthesis and accumulation of some viral protein(s). Recently Scholtissek, Becht & Drzeniek (I967) reported that influenza-virus-induced cell damage can be attributed to the synthesis of a viral protein and Amako & Dales 0967) suggested that Mengo-virus-induced cell damage can be explained on a similar basis. Puromycin is a well-known inhibitor of protein synthesis both in cell-free systems (Yarmolinsky & De la Haba, 1959; Nathans & Lipmann, I96I ) and in intact cells (Rabinovitz & Fisher, 196z). This compound prevents the multiplication of poliovirus in HeLa cells (Levintow et al. I962) and of Mengo virus in L cells (Franklin & Baltimore, 1962). Puromycin has also been used extensively to study the vaccinia-virusinduced biochemical changes in many cell types (Kit, Dubbs & Piekarski, 1963; Joklik, i964; Magee & Bach, I965; Munyon & Kit, 1966 ). The inhibitory effect of puromycin on virus-induced cytopathological changes has been described for poliovirus (Bablanian et al. I965b). Such an effect on vaccinia-virus-induced cytopathological changes has been mentioned, but not documented (Hanafusa, I962). In the present study the relationship between vaccinia-virus-induced cytopathic effects and virus-induced protein synthesis was investigated. It will be shown that vaccinia-virus-induced early cytopathological changes are related to the synthesis of virus-induced protein(s). METHODS Viruses. Two strains of vaccinia virus were used in these studies. The International Health Division strain (lrro) was obtained from the American Type Culture collection as a I0 ~o chorioallantoic membrane suspension. Virus seeds prepared in a continuous line of monkey kidney cells (LLC-MK 2) gave titres of 2 to 4 x Io 7 p.f.u.ml, when assayed on LLC-MK 2 cells. The second vaccinia virus strain (NYC) was obtained as a calf lymph preparation from the New York City Department of Health and passaged on the chorioallantoic membrane of chicken eggs. Seed virus was prepared by infecting monolayer cultures of chick embryo fibroblasts with the preparation of vaccinia virus from the chorioallantoic membrane. Seed virus preparations assayed on LLC-MK 2 cells gave titres of 4 to 7 x Io 7 p.f.u.ml. Cell lines andgrowth media. The LLC-MK 2 continuous monkey kidney cell line was obtained from the American Type Culture collection and was passaged in reinforced Eagle's medium supplemented with IO ~o foetal calf serum (Bablanian, Eggers & Tamm, I965a ). Foetal calf serum was purchased from Microbiological Associates Inc., Bethesda, Maryland. Compounds. Puromycin dihydrochloride and isatin-fl-thiosemicarbazone were purchased from Nutritional Biochemicals Corporation, Cleveland, Ohio. Actinomycin D, sold under the trade name of Cosmegen, was purchased from Merck Sharp and Dohme. The phenylalanine analogue, oc-p-fluorophenylalanine, was purchased from Mann Research Laboratories, Inc., New York. The pyrimidine analogue, 5-fluoro-2"- deoxyuridine was a gift from Dr Duschinsky of Hoffmann-La Roche Inc. All compounds were diluted in reinforced Eagle's medium containing Io ~o foetal calf serum to obtain the desired concentrations. Isatin-fl-thiosemicarbazone was dissolved in acetone at 5 mg.ml, just before use and then diluted in medium to the required concentrations. Infection of cell cultures. Replicate cultures of LLC-MK 2 cells grown in 30 x IO mm.

3 Early vaccinia virus cytopathic effects 53 (Falcon) plastic dishes were infected at a multiplicity of 50: L Virus adsorption was permitted for I hr in a humidified atmosphere of 5 ~o CO~ in air. At I5 rain. intervals the plates were rocked to redistribute the virus on the cells. The virus inoculum was then removed, the plates were washed once with warm phosphate buffered saline (PBS), and 2 ml. of reinforced Eagle's medium with Io ~ foetal calf serum was added to each plate. The plates were returned to the 5 ~o CO~ incubator at 37. At intervals after infection, two Petri-dish cultures were collected for determination of the extent of cell damage and measurement of virus yield. Maximal virus yield (about Ioo p.f.u. cell) was reached at about I9 to 24 hr. Infection of cell cultures in the presence of compounds. LLC-MK 2 cells were infected with vaccinia virus at a multiplicity of 5o: I. Concurrently, replicate cell cultures were infected and treated with compounds at varying concentrations. At the end of a I hr adsorption period, all cultures were washed with warm PBS and refed with 2 ml. of reinforced Eagle's medium with io ~ foetal calf serum or compound dissolved in this medium. The cultures were incubated at 37 in a humidified atmosphere of 5 ~ CO2 in air. The virus yields in 24 hr samples were measured by plaque assay. Measurement of virus yield. Replicate infected cultures of LLC-MK 2 cells were collected at intervals after infection and stored at -2o. When all the cultures had been collected they were allowed to thaw at 37 in a humidified atmosphere of 5 ~ CO2 in air. The adhering cells were scraped off with a silicone rubber policeman, and the cell suspensions transferred to test tubes. Each of these cell suspensions was then treated for I5 sec. at 80 ~o of full power with an ultrasonic generator driving a 'needleprobe' transducer (Bronwill Biosonik II, no. BP-II-4oT). The yield of infective virus was determined by plaque assay in LLC-MK 2 monolayer cultures. After I hr adsorption at 37 the inoculum was removed and the plates were overlaid with 8 ml. of an overlay mixture consisting of equal volumes of ~.8 ~o agar and x 2 concentrated reinforced Eagle's medium with 5 ~o calf serum. Quantification of virus-induced cytopathological changes. The early vaccinia-virusinduced cell rounding was observed with an inverted phase-contrast microscope. Both the rounded and unrounded cells within the area defined by a grid were counted with a I2"5 ocular and a x IO phase objective. The extent of virus-induced cell damage was expressed as a percentage of cells rounded (Bablanian et al. I965a ). Ultraviolet irradiation experiments. The International Health Division strain of vaccinia seed virus was centrifuged for 30 min. at I9,ooo g. The pellets were suspended in PBS and the suspension was treated with ultrasound for 2 min. Virus was placed in plastic Petri dishes (Falcon, 60 x 15 mm.) and irradiated in 2 ml. amounts at a distance of 40 cm. from a Westinghouse germicidal lamp (782 L-3o) of the mercuryvapour type. The energy of the ultraviolet source at this distance was 2I ergssec. ram. ~. Ninety-five per cent of the ultraviolet radiation emitted by this lamp is at the wavelength of 2537 ~,. Replicate cultures of LLC-MK 2 cells grown in 30 x Io mm. (Falcon) plates were infected with the virus or the virus samples which were irradiated for I5, 30, or 45 sec. Virus-induced cell damage was observed at 2 hr after infection. Surviving virus after irradiation was measured by plaque assay.

4 54 R. BABLANIAN RESULTS Kinetics of vaccinia virus multiplication and the development of cytopathological changes Following infection of cells with either the ]HD or the NYC strain (Fig. I, 2), there was a latent period of 5 hr. Between 5 and 9 hr after infection virus growth was exponential. Forty-eight per cent of the cells infected with the md strain of vaccinia 00 z,00 Ii 00 "~1 ' - "~ [ - -~ > r~ m \ 1 t I~'t t I I t t I t I 1 1 I I I I I I~ I I I I I Hours Hours Fig. I Fig. 2 Fig. I. Time course of vaccinia virus md strain multiplication and of the development of virus-induced cell damage in LLC-MK 2 cells. ----, cell damage; ~--A, virus yield. Fig. 2. Time course of vaccinia virus (NYc strain) multiplication and of the development of virusqnduced cell damage in LLC-MK 2 cells. ----, cell damage; A--A, virus yield. virus were rounded by [ hr after infection and by z hr and 40 min. 98 ~ of the cells were rounded. Cells infected by the NvC strain began rounding somewhat later; 2 hr after infection 28 ~ of the cells were affected and by 4 hr after infection Ioo ~o were rounded. These results with LLC-MK 2 cells confirm previous reports that pox viruses can cause marked cytopathologicat changes before production of infectious virus (Brown et al. I959; Hanafusa, I96o; Appleyard et al. I962). In addition, they show that the time course of early virus-induced cell damage varies with different strains of vaccinia virus (Fig. I, 2). Effect of puromycin on vaccinia virus multiplication and on virus-induced cytopathological changes Puromycin at a concentration of 33o gg.ml, completely suppressed the multiplication of the 1riD strain of vaccinia virus for 24 hr after infection (Fig. 3). At 330 Fg.ml. the compound also completely prevented the development of virus-induced cytopathological changes which in untreated infected cultures were maximal by 2 to 3 hr after infection. Even after 24 hr of infection and treatment LLC-MK 2 cells showed no

5 Early vaccinia virus cytopathie effects 55 cytopathic effects. Puromycin at a concentration of 33 Fg.ml. decreased the yield of virus by 88 ~, but virus-induced cytopathological changes developed with no delay as compared to infected but untreated cultures. The early cytopathic effects of vaccinia virus (NYC strain) were completely prevented by 220zg.ml. of puromycin, but 33zg. ml. of the drug had no effect on the rate of development of early virus-induced cell damage. =o 100< I I i I I i l e., et ~ - ~. - +f : 0.1 I I I I I I Concentration of puromycin (#g.ml.) Fig. 3. Inhibition of vaccinia virus (IHD) multiplication by puromycin. Table I. The effect of removal of puromycin or actinomycin D from infected cultures on vaccinia virus yield Treatment No compound Virus and puromycin 330zg.ml. Virus and puromycin 330 #g.ml. (puromycin removed 4 hr after infection) Virus and actinomycin 5zg.ml. Virus and actinomycin 5*g.ml. (actinomycin removed 4 hr after infection) Virus yield (p.f.u.ml., 24 hr after Percentage of infection)* control 8"4 x io 6 ioo 4'7 x iot o.6 I'OX IO 7 II 9 3" "4 I'I 10 s 13 * The I hr background value of virus was 2"4 x io 5 p.f.u.ml. The effect of removal of puromycin from uninfected and infected treated cultures Since 33ozg.ml. of puromycin was needed to inhibit vaccinia-virus-induced early cell damage 0DrI strain) it was decided to see what effect this concentration of the compound would have on uninfected and infected LLC-MK 2 cells when the compound was removed. LLC-MK 2 ceils treated with 33o Fg.ml. of puromycin for 4 hr,

6 56 R. BABLANIAN after which the compound was removed by washing, recovered completely and divided at the same rate as untreated control cells. Replicate cultures were infected and either treated or not with puromycin (33o Fg. ml.). Four hr after infection, when untreated-infected cells would all have been rounded for at least ~ hr, puromycin was removed from two infected-treated cultures. The cultures were washed three times with 2 ml. of medium, and then fed with 2 ml. of fresh medium. Virus-induced cell damage in such cultures was estimated at frequent intervals after the removal of puromycin and virus yields were measured 24 hr after infection. The rate of cell rounding in untreated infected cultures was also determined. In untreated cells about 3 hr was required before 97 ~ of the cells showed virus-induced ~o loo 60 ~ 40 " 20 > I I jf -, I I I I 0 ~ ~0 I I I I l l l 1 2 Hours I I I l I I I I.~ I I I I ~~1 I I Fig. 4. Time course of vaccinia-virus-induced cytopathological changes in the absence, or after the removal, of puromycin (330zg.ml) from LLC-MK 2 cells. O-- --O, cell damage; A A, cell damage after removal of drug. Arrow indicates removal of puromycin. morphological damage (Fig. 4). However, when puromycin was removed from infectedtreated cultures 4 hr after infection, virus-induced cytopathic effects appeared t5 min. after the removal of the drug, and 45 rain. later 95 ~o of the cells showed viral cytopathic effects. The presence of puromycin for 4 hr in infected cultures had no effect on the yield of virus from such cells measured 20 hr later (Table I). Effect of actinomycin D on vaccinia virus multiplication and on virus-induced cytopathological changes Actinomycin D inhibits vaccinia virus replication in cultured cells (Reich et al. I96x ; Shatkin, I963b ). The effect of this compound on virus-induced cytopathological changes has not been reported. Actinomycin D inhibited the yield of vaccinia virus 99 ~ at the two concentrations used, 5 #g.ml. and 0"5zg.ml. (Table 2). Three hr after infection, when Ioo?o of the untreated infected cells showed cytopathological changes, actinomycin D (5 Fg.mI.) protected 9o ~ of the cells from virus-induced morphological changes. However, viral cytopathic effects occurred almost as rapidly in the presence of actinomycin D o'5 Fg.ml. as in its absence. Contrary to the results obtained with puromycin, LLC-MK 2 cells treated with actinomycin D, 5 Fg.ml., degenerated within 15 to 2o hr after treatment regardless of whether the compound was removed by washing 4 hr after treatment or not. Furthermore, the 24 hr virus yields from such cultures were only about Io ~ of the maximal

7 Early vaccinia virus cytopathic effects 57 yields attained (Table I). Thus, unlike the effect of puromycin, that of actinomycin D cannot be entirely reversed. The lack of inhibition of vaccinia-virus-induced early cytopathic effects by 5-fluoro-2'- deoxyuridine, p-fluorophenylalanine, and isatin-fl-thiosemicarbazone 5-fluoro-2'-deoxyuridine (Salzman, 196o), p-fluorophenylalanine, (Salzman, Shatkin & Sebring, I963 ) and isatin-fl-thiosemicarbazone (Thompson et al. 1953) all inhibit poxvirus multiplication. Even though isatin-?-thiosemicarbazone inhibits Table 2. The effect of actinomycin D on vaccinia virus growth and virus-induced morphological changes in LLC-MK 2 cells Virus yield Inhibition Cells damaged (p.f.u.ml., 24 hr after of virus yield 3 hr after infection Treatment infection)* (~) (7oo) No compound I'O IO 7 -- IOO Actinomycin D (5zg.ml.) Actinomycin D (0"5#g.ml.) 5"5 Io 4 l "5 x io 8 99"7 99"2 8 IOO * The I hr background value of virus was 3"5 x io 5 p.f.u.ml. Table 3. The effect of 5-fluoro-2"-deoxyuridine, p-fluorophenylalanine and isatin-flthiosemicarbazone on vaccinia virus growth and virus-induced morphological changes in LLC-MK 2 cells Virus yield Inhibition Cells damaged, (p.f.u.ml., of virus 3 hr after 24 hr after yield infection Treatment infection)* (%) (%) No compound 3"5 x io 7 -- IOO 5-fluoro-2'-deoxyuridine (2'5 #g.ml.) 9"6 x lo t 99"7 IOO p-fluorophenylalanine (350#g. nal.) No compound 1.o x 106 5'9 x io e 97" oo ioo isatin-fl-thiosemicarbazone (5zg.ml.) 5"1 IO 4 99'I ioo * The I hr background values of virus were 3'4 x lo 5 and 1-4 x lo 5 p.lu.ml. multiplication of infectious virus, poxvirus-induced early cytopathic effects were not prevented by the compound (Appleyard et al. I962). Experiments were made to determine the effects of these compounds on the multiplication and cytopathic effects of vaccinia virus in LLC-MK 2 cells. Virus-induced cytopathic effects in the presence of 5-fluoro-'-deoxyuridine (2"5zg.ml.), p-fluorophenylalanine (35ozg.ml.) and isatin-fl-thiosemicarbazone (5zg.ml.) were maximal 3 hr after infection, although all three compounds inhibited production of infectious virus (Table 3). The effect of ultraviolet irradiation on virus infectivity and virus-induced cytopathology Poxviruses exposed to ultraviolet radiation lose their infectivity more rapidly than their ability to cause cell damage (Brown et al. I959; Hanafusa, 1960; Appleyard et al. 1962). The previous results were confirmed using the md strain of vaccinia virus to infect LLC-MK 2 cells. Although the infectivity of the virus, as measured by plaque formation, was reduced by 8o ~o after I5 sec. of irradiation, early cytopathic effects occurred in almost 90 ~ of the ceils. Even after 45 sec. of ultraviolet irradiation, when

8 5 8 R. BABLANIAN less than I ~ of the initial infectivity of the virus remained, 41 ~o of the cells showed virus-induced cytopathological effects. Ultraviolet irradiation therefore reduced the plaque-forming ability of vaccinia virus more rapidly than thc ability of the virus to cause cell damage (Fig. 5). 100~ -_ o ~ : ' "~'.~ 0 ~:~ ~ = r~ T-, U.v. irradiation (sec.) Fig. 5. The effect of ultraviolet irradiation on vaccinia virus infectivity and cytopathogenicity. O----O, cell damage; A------A, surviving virus. The effect of heat on viral infectivity and cytopathogenicity Previous reports have indicated that heat-inactivated vaccinia virus loses its infectivity (Fenner et al. 1959) and its ability to cause early cytopathic effects (Brown et al. 1959; Hanafusa, 196o). Heat-inactivated virus causes cell damage 15 hr after infection, but the type of virus-induced cell damage is quite different from cell damage caused by either active or u.v.-inactivated virus (Hanafusa, 196o). The mn strain of vaccinia virus, diluted to give a multiplicity of 50, was heated for I hr at 56 and inoculated to LLC-MK 2 cells. Cells exposed to heated virus did not show any morphological changes for 24 hr, when virus multiplication could not be demonstrated. DISCUSSION The results of the present investigation suggest that the vaccinia-virus-induced early cytopathic effects are related to the active synthesis of one or several virus-induced proteins. The evidence may be summarized as follows: vaccinia-virus-induced early cytopathic effects, manifested by the rounding of cells, appear by 1 hr after infection and, depending on the vaccinia virus strain, are complete by 2 or 4 hr after infection. Chemical inhibitors of vaccinia virus reproduction which do not prevent virus-induced cell damage, such as 5-fluoro-2'-dexoyuridine (Salzman, i96o), p-fluorophenylalanine (Salzman et al. I963), sodium azide (Brown et al. 1959) and isatin-p-thiosemicarbazone (Appleyard et al ) all allow the synthesis of some viral antigens. Shatkin (1963 a)

9 Early vaccinia virus cytopathic effects 59 showed that 5-fluoro-2'-deoxyuridine does not affect the initial rate of viral protein synthesis. Loh & Payne (1965) demonstrated that p-ftuorophenylalanine at a high concentration (35o #g.ml.) inhibits production of infectious vaccinia virus, viral DNA, nucleoprotein (NP) antigen and viral haemagglutinin, but does not inhibit the formation of the LS antigen. Appleyard et al (1965) have shown that isatin-fl-thiosemicarbazone allows the synthesis of the ' early' vaccinia-virus-induced antigens. Sodium azide, which inhibits vaccinia virus production, allows the synthesis of some poxvirusinduced antigens (Appleyard et al. 1962). It is also known that u.v.-irradiated poxvirus which has lost its infectivity but not its 'toxicity' for cells (Brown et al. 1959; Hanafusa, 196o; Appleyard et al I962) is capable of producing some viral antigens (Appleyard et al. 1962). All these data indicate that a relationship exists between the restricted synthesis of virus-specific products and early virus-induced cytopathic effects. The results with puromycin suggest that the so-called viral 'toxic' effects can be completely prevented when protein synthesis is inhibited by an adequate concentration of puromycin and that a smaller dose of the compound will allow a partial cycle of vaccinia virus multiplication, resulting in the synthesis of some virus-induced proteins which lead to the rapid destruction of the infected cells. The present experiments, however, do not definitely discriminate between virus-coded proteins or cell-coded proteins as possible causative agents in virus-induced cell damage since puromycin inhibits all protein synthesis, both viral and cellular. It is interesting to note, however, that in the same cell line (LLC-MK z) a smaller amount of puromycin (22ozg.ml.) is sufficient to inhibit the early virus-induced cytopathic effects caused by the ~,~'c strain of vaccinia virus. This observation may suggest that early virus-induced cell damage might be coded for by the virus. The results from the puromycin removal experiments allow the following conclusions to be drawn. (I) Puromycin, at a concentration of 330 #g.ml., does not irreversibly damage LLC-MK 2 cells nor is there any adverse effect on virus synthesis when the drug is removed by washing 4 hr after treatment. (2) The fact that virus cytopathic effects appear within 15 rain. after the removal of puromycin suggests that in the presence of the drug some viral messenger(s) are made which code for virus protein(s) responsible for the early morphological cell damage. This conclusion is also supported by recent evidence that virus-directed RNA synthesis can take place at the core stage in virus uncoating (Munyon & Kit, I966; Kates & McAuslan, I967; Woodson, 1967). The results with actinomycin D support the previous conclusion that protein synthesis is necessary for the development of virus-induced cell damage. Actinomycin D inhibits RNA synthesis (Reich et al , and without the synthesis of vaccinia virus messenger RNAs the production of viral proteins cannot occur. The results of the experiment with u.v.-irradiation (Fig. 5) suggest that virus infectivity follows a one-hit curve whereas virus-induced early cytopathic effects do not. The chances for inactivating any one of the cistrons on a polycistronic viral DNA (which could abolish infectivity) are much greater than the chances for inactivating one or a few cistrons which presumably code for the protein(s) responsible for cell damage. Heat-inactivated poxvirus does not multiply in cultured cells (Joklik et al. 196o) and does not cause early virus cytopathic effects (Hanafusa, I96o). Heat-inactivated virus penetrates cells at the same rate as unheated virus (Dales & Kajioka, I964), but

10 60 R. BABLANIAN it is not uncoated (Joklik, 1962). Thus, from these findings it may be concluded that the mere introduction of virus particles into the cell does not bring about early cytopathic effects. From all the available information it seems rather that the early virus-induced cell damage results from the synthesis of one or more virus-induced proteins. If this is so, the term viral 'cytotoxic' effect is inappropriate. The author wishes to acknowledge the technical assistance of Mr William H. Lilliewood. REFERENCES AMAKO, K. & DARES, S. (I967). Cytopathology of mengovirus infection. I. Relationhip between cellular disintegration and virulence. Virology 32, 2ot. AvvrrY~a~, G., HUME, V. B. M. & WESaWCOOD, J. C. N. (1965). The effect of thiosemicarbazones on the growth of rabbitpox virus in tissue culture. Ann. N.. Acad. Sci. 13o, 92. AVPLE ~a~d, G., WESTWOOD, J. C. N. & ZWARTOUW, H. T. 0962). The toxic effect of rabbitpox virus in tissue culture. Virology 18, 159. B~LANmN, R., E~or~, H. J. & TA~, I. (I965a). Studies on the mechanism of poliovirus-induced eell-damage. I. The relation between poliovirus-induced metabolic and morphological alterations in cultured cells. Virology 26, IOO. B~NmN, R., Eccrv, s, H. J. & TAMM, I. 0965b). Studies on the mechanism of poliovirus-induced cell damage. II. The relation between poliovirus growth and virus-induced morphological changes in cells. Virology 26, I I4. BrRNKOVF, H., NISei, M. &ROSlN, A. (1959). Effect of active and inactive vaeeinia virus preparations on human amnion cell cultures. J. Immun. 83, 635. BROWN, A., MA~ASI, S. A. & OffICER, J. E. (1959). The 'toxic' activity of vaccinia virus in tissue culture. J. infect. Dis. xo4, I93. DALES, S. & K~1or,~, R. (1964). The cycle of multiplication of vaccinia virus in Earle's strain L cells. I. Uptake and penetration. Virology ~-4, 278. EASTERBROOK, K. B Analysis of the early stages of vaccinia virus infection in KB cells using sodium azide. Virology x$, 417. FEN~qER, F., HOLMES, I.H., Jor~n, W.K. & WOODROOFr, G.M. 0959). Reactivation of heatinactivated poxvirus: a general phenomenon which includes the fibroma-myxoma virus transformation of Berry and Dedrick. Nature, Lond. 183, 134o. FRA~KLrN, R. M. & BALTIMORE, D. (I962). Patterns of macromolecular synthesis in normal and virusinfected mammalian cells. Cold Spring ttarb. Syrup. quant. Biol. 27, 175. HANArUSA, H. (196o). Killing of L cells by heat and u.v.-inaetivated vaecinia virus. Biken's J. 3, I9x. HAa~ArUSA, H. (I962). Factors involved in the initiation of multiplication of vaccinia virus. Cold Spring Harb. Syrup. quant. Biol. 27, 209. JOKL~K, W. K. 0962). Reactivation of poxviruses: fate of reaetivable virus within the cell. Nature, Lond. 196, 556. Jomox, W. K. (I964). The intracellular uncoating of Poxvirus DNA. II. The molecular basis of the uncoating process. J. molec. Biol. 8, 277. JOKLIK, W. K. (1966). The poxviruses. Bact. Rev. 3o, 33. JOIrJ.IK, W. K., WOODROOFE, G. M., HOLMES, I. H. & FENNER, F. (1960). The reactivation of poxviruses. I. The demonstration of the phenomenon and technique of assay. Virology ix, 168. KA~S, J. R. & McAUSLAN, B. R. (I967). Messenger RNA synthesis by a 'coated' viral genome. Proc. natn. Acad. Sci., U.S.A. 57, 314. KtT, S., D~rBBS, D. R. & PIEKARSKI, L. J. (t963). Inhibitory effects of puromycin and fluorophenylalanine on induction of thymidine kinase by vaccinia infected L cells. Biochem. biophys. Res. Commun. ix, I76. LEVrNTow, L., THOREN, M. M., DARNELL, J. E. Jmq. & HOOeER, J.L. (r96z). Effect of p-fluoro phenylalanine and puromycin on the replication of poliovirus. Virology x6, 22o.

11 Early vaccinia virus cytopathic effects Loll, P. C. & PAYNE, F. E. (1965). Effect of p-fluorophenylalanine on the synthesis of vaccinia virus. Virology 25, 560. MACEE, W. E. & BACH, M. K. (I965). Biochemical studies on the antiviral activities of the isatin-fl-thiosemicarbazones. Ann. N.Y. Acad. Sci. x3o, 8o. MUNYON, W. H. & KIT, S. (I966). Induction of cytoplasmic ribonucleic acid (RNA) synthesis in vaccinia-infected LM cells during inhibition of protein synthesis. Virology 29, 303. NATHANS, D. & Ln~ANN, F. (I96I). Amino acid transfer from aminoacyl ribonucleic acids to protein on ribosomes of Escherichia coli. Proc. natn. Acad. Sci. U.S.A. 47, 497. RAmNOVlTZ, M. & FisrmR, J. M. (I962). A dissociative effect of puromycin on the pathway of protein synthesis by Ehrlich ascites tumour cells. J. biol. Chem. 32x, 139. REICH, E., FRANKLIN, R. M., SHATKIN, A. J. & TATUM, E. L. (196I). Effect of actinomycin D on cellular nucleic acid synthesis and virus production. Science, N.Y. x34, 556. SALZMAN, N. P. (I96O). The rate of formation of vaccinia deoxyribonucleic acid and vaccinia virus. Virology xo, I5O. SALZMAN, N. P., SHATKIN, A. J. & SESRt~O, E. D. (I963). Viral protein and DNA synthesis in vaccinia virus-infected HeLa cell cultures, tirology x9, 542- SCnOLTISSEK, C., BECHT, H. & DRZENmK, R. (1967). Biochemical studies on the cytopathic effect of influenza viruses. J. gen. Virol. x, 219. SHATKIN, A. J. (1963a). The formation of vaccinia virus protein in the presence of 5-fluorodeoxyuridine. Virology 2o, 292. SHATKIN, A. J. (1963 b). Actinomycin D and vaccinia virus infection of HeLa cells. Nature, Lond. x99, 357. THOMPSON, R. L., DAVIS, J., RUSSELL, P. B. & HITCmNGS, G. H. (I953). Effect of aliphatic oxime and isatin thiosemicarbazones on vaccinia infection in the mouse and in the rabbit. Proc. Soc. exp. Biol. Med. 84, 496. WOODSON, B. (I967). Vaccinia mrna synthesis under conditions which prevent uncoating. Biochem. biophys. Res. Commun. 27, I69. YARMOLINSKY, M. B. & DE LA HABA, G. L. (I959)- Inhibition by puromycin of amino acid incorporation into protein. Proc. HatH. Acad. Sci. U.S.A. 45, (Received 23 November 1967) 6I

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