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The 5' End of Poliovirus Mrna Is Not Capped Withm7g(5'

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The 5' End of Poliovirus Mrna Is Not Capped Withm7g(5' Proc. Nat. Acad. Sci. USA Vol. 73, No. 2, pp. 375-380, February 1976 Biochemistry The 5' end of poliovirus mRNA is not capped with m7G(5')ppp(5')Np (polyribosomes/fingerprints) AKIo NOMOTO, YUAN FON LEE, AND ECKARD WIMMER Department of Microbiology, School of Basic Health Sciences, State University of New York at Stony Brook, Stony Brook, N.Y. 11794 Communicated by Bentley Glass, November 17,1975 ABSTRACT Poliovirus was grown in HeLa cells in the lated from polyribosomes of infected HeLa cells. We were presence of phosphorus-32 and actinomycin D. Three to four unable to identify a capping group in the viral mRNA, but hours after infection, viral mRNA was recovered from polyri- obtained evidence that suggests that pUp is the 5' end. To bosomes and its "identity verified by two-dimensional gel electrophoresis of RNase Ti digests. Digestion of the viral our knowledge this is the only mRNA so far isolated from a [-P32PmRNA with RNase T2 and separation of the products by mammalian cell that is uncapped. ion exchange chromatography at pH 5 yielded pUp as possi- ble 5' terminus but no "capping group" of the structure m7G(5')ppp(5')Np. Total cytoplasmic []PJRNA of HeLa cells, MATERIALS AND METHODS on the other hand, was found to contain capping groups. Nei- Poliovirus type 1 (Mahoney) was grown and labeled in spin- ther the capping group nor ppNp or pppNp was found in an ner cultures of HeLa S3 cells, and its RNA was extracted, as RNase T2 digest of poliovirion [ PJRNA, in agreement with published previously (1, 18). Poliovirus [32P]mRNA was iso- previous results [Wimmer, E. (1972) J. MoL. Biol. 68, 537-5401. The data indicate that 5'-terminal m7G(5')ppp(5')Np is absent lated as follows: 100 ml of HeLa cells (4 X 106 cells per ml) from poliovirus RNAs and, therefore, is not involved in polio- were infected with 30-50 plaque-forming units per cell of virus protein synthesis. poliovirus (19) and incubated at 370. Ninety minutes after infection the cells were washed and suspended in ice-cold mRNAs of a number of animal viruses contain an unusual phosphate-free medium containing 5% dialyzed calf serum group of methylated nucleotides with the general structure at 4 X 106 cells per ml. The cells were kept at 00 for 90 min m7G(5')ppp(5')Nmp (2) at the 5' terminus. This group, (1), then mixed with actinomycin D (5 gg/ml) and carrier- which we shall refer to as a "capping group" (3, 4), has been free phosphorus-32 (0.6 mCi/ml), and incubated at 370. found in mRNAs of cytoplasmic polyhedrosis virus (2), After a total incubation time at 370 of 3.2-4 hr the cells human reovirus (5), vaccinia virus (6, 7), and vesicular sto- were washed twice with ice-cold 0.14-buffer (0.14 M NaCl, matitis virus (8). More recent reports indicate that the cap- 0.01 M KC1, 0.01 M Tris.HCl, pH 7.5, 1.5 mM Mg9l2), sus- ping group is present in mRNA of every mammalian cell pended in 6 ml of 0.14-buffer, and layered in portions of 2 that has been analyzed so far, for example, in mRNA of ml onto stepwise sucrose gradients. The sucrose gradients HeLa cells (4, 9) mouse myeloma cells (10), rabbit reticulo- contained (from bottom to top): 2 ml of 60% sucrose in RSB cytes (11), and monkey kidney cells (12). Finally, viral RNAs + Mg buffer (0.01 M KCI, 0.01 M Tris-HCI, pH 7.5, 1.5 mM that are synthesized in the nucleus are also capped at the 5' Mg9l2), 30 ml of a gradient (15-30%) of sucrose in RSB + end, as has been shown for mRNA of simian virus 40 (12) Mg buffer, and 3 ml of 10% sucrose, 1% deoxycholate, 1% and for Rous sarcoma virus RNA (13). Brij 58 in RSB + Mg buffer. The gradients were spun in a Available evidence suggests that the capping group plays Spinco SW 27 for 90 min at 26,000 rpm and 40 and were an important role in host cell and viral protein synthesis (11, fractionated at 40. The contents of each fraction were moni- 14), presumably during the formation of the initiation com- tored for absorbance at 260 nm and radioactivity. Fractions plex (15). While the capping group may be universally containing polyribosomes were combined, mixed with 1M found in mRNA of eukaryotic cells, a crucial question re- volume of 0.3 M Mg9l2 (20), and kept for 30 min at 00. Pre- mains unanswered: is the presence of 5'-terminal cipitates of polyribosomes were collected by centrifugation, m7G(5')ppp(5')Nmp obligatory for a mRNA to function in dissolved in 0.02 M EDTA, 1% sodium dodecyl sulfate, and protein synthesis? If so, all species of mRNA translated in treated three times with phenol/chloroform (18, 21). The the cytoplasm should be terminated with the capping group. deproteinized RNA was sedimented through a sucrose gradi- Poliovirus contains a single-stranded RNA genome which, ent (15-30%) in 0.1 M NaCl, 0.01 M Tris-HCl, pH 7.5, 1 mM immediately after penetration and uncoating of the virus in EDTA, 0.5% sodium dodecyl sulfate. 35S RNA was collected the host cell, functions as mRNA in viral protein synthesis and used for further analyses. (for reviews see refs. 16 and 17). Earlier studies have shown Total cytoplasmic HeLa cell [32P]RNA was prepared from that the poliovirion RNA contains a 5' end with the general cells that had been labeled with 32P (0.3 mCi/ml) in the structure pNp (1). The terminal base was found to be adeno- presence of 0.05 ,gg/ml of actinomycin D (4, 21). RNA sedi- sine (1), although recently, alkaline digests of virion RNA menting between 10 and 28 S was isolated by zonal centrifu- yielded more pUp than pAp as possible 5'-termini (Jacobi gation. and Wimmer, unpublished). Lack of the capping group in Other procedures are outlined in the legends to the fig- poliovirion RNA does not exclude the possibility that ures. m7G(5')ppp(5')Nmp is involved in poliovirus protein synthe- sis, since cell-free extracts have been found to block and methylate unmethylated viral mRNAs (11, 14). Thus, polio- RESULTS virus RNA might be modified in the cytoplasm of HeLa Isolation of Poliovirus mRNA. During infection with po- cells prior to or during complex formation with ribosomes. liovirus, cellular polyribosomes are replaced by the much We have, therefore, analyzed poliovirus-specific mRNA iso- larger virus-specific polyribosomes, resulting in an inhibition 375 376 Biochemistry: Nomoto et al. Proc. Nat. Acad. Sci. USA 73 (1976) 25] 28S 1S 4S 12.0 I I I c. o 6 II 6 I lo a sO E ot,) 0(o 01 N pi5, .L 10- -40 0 5 10 I5 20 25 5- FRACTIONS FIG. 2. Zonal centrifugation of phenol/chloroform-treated po- lyribosomes. Deproteinized polyribosomal RNA was sedimented through 15-30% sucrose as described in Materials and Methods. 0 5 10 15 20 25 print was prepared of [32P]mRNA isolated from the polyri- FRACTIONS bosomal fractions, an identical pattern was obtained (Fig. FIG. 1. Centrifugation of poliovirus-infected, 32P-labeled SB). All spots of the large oligonucleotides of Fig. SA and B HeLa cells through a stepwise sucrose density gradient. The top are superimposable. These fingerprints not only identify the layer of the gradient contained 1% deoxycholate, 1% Brij-58. The labeled RNA found in polyribosomal fractions as poliovirus bottom of the tube is at the left. Material indicated by the double- plus-strand RNA but also show that the viral mRNA is free headed arrow was collected and analyzed. of contamination by labeled cellular RNA or polio minus- strands. End Group Analysis of the mRNAs. Analyses for the of host-cell protein synthesis. This process is accelerated in capping group were performed according to established pro- the presence of actinomycin D (16, 17). Fig. 1 shows the sed- cedures (1, 2) in which RNA is digested exhaustively with al- imentation profile of a detergent lysate of infected HeLa kali or RNase T2. Nucleotides are separated by column cells. The cells were labeled from 90 to 210 min after infec- chromatography on DEAE-cellulose. Triethylammonium tion with phosphorus-32 in the presence of 5 ttg/ml of acti- acetate (EtsN.HOAc), pH 5, was used as eluent because (i) nomycin D. As found previously (16, 17), the peak at 150 S excellent separation of nucleotides was achieved under these (fraction 18) represents newly synthesized poliovirions. conditions (Fig. 4A), (ii) the capping group might be de- Virus-specific polyribosomes sediment faster than virions, graded at alkaline pH (26), and (iii) Et3N-HOAc is volatile with S-values between 150 and 400 (16, 17). From the su- crose gradient of Fig. 1 we isolated fractions as indicated by the double-headed arrow. Viral polyribosomes in these frac- A 9 B tions precipitated in 30 mM MgCl2 (20) and yielded 35S sin- gle-stranded RNA when treated with EDTA and phenol. As can be seen in Fig. 2, most of the 32P-labeled RNA recov- ered from deproteinized polyribosomes sediments faster 1 , )kt .: than 28S ribosomal RNA, although some RNA, sedimenting *'*4I slower than 28 S, can also be observed. We consider the 40 4. RNA to be breakdown of the * kk slowly sedimenting products >. - }t J viral mRNA and not contaminations of other RNA (see #,i '- 9s:~1S ''0* below). It is unlikely that an appreciable amount of the la- -zI 4 ,* beled RNA in Fig.
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