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. 1972 Dec;10(6):1098–1108. doi: 10.1128/jvi.10.6.1098-1108.1972

Transient Inhibition of Polyoma Virus Synthesis by Sendai Virus (Parainfluenza I) II. Mechanism of the Interference by Inactivated Virus 1

Gary L Smith a,2, Richard A Consigli a
PMCID: PMC356589  PMID: 4345489

Abstract

The mechanism of the transient inhibition of polyoma virus synthesis by betapropiolactone-inactivated Sendai virus was studied. Polyoma virus early functions did not appear to be affected, although deoxyribonucleic acid (DNA) and structural protein synthesis were inhibited 60 and 35% respectively. The inhibition of macromolecular synthesis was not sufficient to account for the 90% inhibition of infectious progeny formation. Encapsidation of polyoma DNA into mature virions appears to be completely inhibited after superinfection by beta-propiolactone-inactivated Sendai virus. Ultraviolet irradiation of live or beta-propiolactone-inactivated Sendai virus preparations abolishes the interfering capacity, indicating that a functional Sendai virus ribonucleic acid molecule is the interfering component.

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Selected References

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  1. Aubertin A. M., Guir J., Kirn A. The inhibition of vaccinia virus DNA synthesis in KB cells infected with frog virus 3. J Gen Virol. 1970 Aug;8(2):105–111. doi: 10.1099/0022-1317-8-2-105. [DOI] [PubMed] [Google Scholar]
  2. Aula P., Nichols W. W. Lysosomes and virus induced chromosomes breaage. Exp Cell Res. 1968 Aug-Sep;51(2-3):595–601. doi: 10.1016/0014-4827(68)90147-x. [DOI] [PubMed] [Google Scholar]
  3. BALUDA M. A. Homologous interference by ultraviolet-inactivated Newcastle disease virus. Virology. 1957 Aug;4(1):72–96. doi: 10.1016/0042-6822(57)90044-2. [DOI] [PubMed] [Google Scholar]
  4. BALUDA M. A. Loss of viral receptors in homologous interference by ultraviolet-irradiated Newcastle disease virus. Virology. 1959 Mar;7(3):315–327. doi: 10.1016/0042-6822(59)90201-6. [DOI] [PubMed] [Google Scholar]
  5. BUKRINSKAYA A. G., ZHDANOV V. M. SHORTENING BY ACTINOMYCIN D OF LATENT PERIOD OF MULTIPLICATION OF SENDAI VIRUS. Nature. 1963 Nov 30;200:920–921. doi: 10.1038/200920a0. [DOI] [PubMed] [Google Scholar]
  6. Bourgaux P., Bourgaux-Ramoisy D. Is a specific protein responsible for the supercoiling of polyoma DNA? Nature. 1972 Jan 14;235(5333):105–107. doi: 10.1038/235105a0. [DOI] [PubMed] [Google Scholar]
  7. Bratt M. A., Rubin H. Specific interference among strains of Newcastle disease virus. II. Comparison of interference by active and inactive virus. Virology. 1968 Jul;35(3):381–394. doi: 10.1016/0042-6822(68)90217-1. [DOI] [PubMed] [Google Scholar]
  8. Bukrinskaya A. G., Zhdanov V. M., Vorkunova G. K. Fate of Sendai virus ribonucleoprotein in virus-infected cells. J Virol. 1969 Aug;4(2):141–146. doi: 10.1128/jvi.4.2.141-146.1969. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Choppin P. W., Holmes K. V. Replication of SV5 RNA and the effects of superinfection with poliovirus. Virology. 1967 Nov;33(3):442–451. doi: 10.1016/0042-6822(67)90119-5. [DOI] [PubMed] [Google Scholar]
  10. Consigli R. A., Minocha H. C., Abo-Ahmed H. Multiplication of polyoma virus. II. Source of constituents for viral deoxyribonucleic acid and protein synthesis. J Bacteriol. 1966 Sep;92(3):789–791. doi: 10.1128/jb.92.3.789-791.1966. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Consigli R. A., Minocha H. C., Abo-Ahmed H. The effect of 5-fluoro-deoxyuridine on the replication of viral DNA and synthesis of polyoma capsid protein. J Gen Virol. 1968 May;2(3):437–441. doi: 10.1099/0022-1317-2-3-437. [DOI] [PubMed] [Google Scholar]
  12. Dales S., Silverberg H. Controlled double infection with unrelated animal viruses. Virology. 1968 Mar;34(3):531–543. doi: 10.1016/0042-6822(68)90072-x. [DOI] [PubMed] [Google Scholar]
  13. Doyle M., Holland J. J. Virus-induced interference in heterologously infected HeLa cells. J Virol. 1972 Jan;9(1):22–28. doi: 10.1128/jvi.9.1.22-28.1972. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. EAGLE H. Amino acid metabolism in mammalian cell cultures. Science. 1959 Aug 21;130(3373):432–437. doi: 10.1126/science.130.3373.432. [DOI] [PubMed] [Google Scholar]
  15. Ensminger W. D., Tamm I. The step in cellular DNA synthesis blocked by Newcastle disease or mengovirus infection. Virology. 1970 Jan;40(1):152–165. doi: 10.1016/0042-6822(70)90387-9. [DOI] [PubMed] [Google Scholar]
  16. Frearson P. M., Crawford L. V. Polyoma virus basic proteins. J Gen Virol. 1972 Feb;14(2):141–155. doi: 10.1099/0022-1317-14-2-141. [DOI] [PubMed] [Google Scholar]
  17. Freda C. E., Buck C. A. System of double infection between vaccinia virus and mengovirus. J Virol. 1971 Sep;8(3):293–302. doi: 10.1128/jvi.8.3.293-302.1971. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Fuchs P., Kohn A. Nature of transient inhibition of deoxyribonucleic acid synthesis in HeLa cells by parainfluenza virus 1 (Sendai). J Virol. 1971 Nov;8(5):695–700. doi: 10.1128/jvi.8.5.695-700.1971. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Giorno R., Kates J. R. Mechanism of inhibition of vaccinia virus replication in adenovirus-infected HeLa cells. J Virol. 1971 Feb;7(2):208–213. doi: 10.1128/jvi.7.2.208-213.1971. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. HOLLAND J. J. INHIBITION OF HOST CELL MACROMOLECULAR SYNTHESIS BY HIGH MULTIPLICITIES OF POLIOVIRUS UNDER CONDITIONS PREVENTING VIRUS SYNTHESIS. J Mol Biol. 1964 Apr;8:574–581. doi: 10.1016/s0022-2836(64)80012-7. [DOI] [PubMed] [Google Scholar]
  21. Hancock R., Weil R. Biochemical evidence for induction by polyoma virus of replication of the chromosomes of mouse kidney cells. Proc Natl Acad Sci U S A. 1969 Aug;63(4):1144–1150. doi: 10.1073/pnas.63.4.1144. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Hirt B. Selective extraction of polyoma DNA from infected mouse cell cultures. J Mol Biol. 1967 Jun 14;26(2):365–369. doi: 10.1016/0022-2836(67)90307-5. [DOI] [PubMed] [Google Scholar]
  23. Huang A. S., Baltimore D. Defective viral particles and viral disease processes. Nature. 1970 Apr 25;226(5243):325–327. doi: 10.1038/226325a0. [DOI] [PubMed] [Google Scholar]
  24. Huang A. S., Wagner R. R. Defective T particles of vesicular stomatitis virus. II. Biologic role in homologous interference. Virology. 1966 Oct;30(2):173–181. doi: 10.1016/0042-6822(66)90093-6. [DOI] [PubMed] [Google Scholar]
  25. Huang A. S., Wagner R. R. Inhibition of cellular RNA synthesis by nonreplicating vesicular stomatitis virus. Proc Natl Acad Sci U S A. 1965 Dec;54(6):1579–1584. doi: 10.1073/pnas.54.6.1579. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Iwata A., Consigli R. A. Effect of phleomycin on polyoma virus synthesis in mouse embryo cells. J Virol. 1971 Jan;7(1):29–40. doi: 10.1128/jvi.7.1.29-40.1971. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Joklik W. K., Merigan T. C. Concerning the mechanism of action of interferon. Proc Natl Acad Sci U S A. 1966 Aug;56(2):558–565. doi: 10.1073/pnas.56.2.558. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Kato H., Sandberg A. A. Cellular phase of chromosome pulverization induced by Sendai virus. J Natl Cancer Inst. 1968 Nov;41(5):1125–1131. [PubMed] [Google Scholar]
  29. Katz E., Moss B. Formation of a vaccinia virus structural polypeptide from a higher molecular weight precursor: inhibition by rifampicin. Proc Natl Acad Sci U S A. 1970 Jul;66(3):677–684. doi: 10.1073/pnas.66.3.677. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Khare G. P., Consigli R. A. Cytologic studies in polyoma virus-infected mouse embryo cells. Am J Vet Res. 1967 Sep;28(126):1527–1536. [PubMed] [Google Scholar]
  31. Khare G. P., Consigli R. A. Multiplication of Polyoma Virus I. Use of Selectively Labeled (H) Virus to Follow the Course of Infection. J Bacteriol. 1965 Sep;90(3):819–821. doi: 10.1128/jb.90.3.819-821.1965. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Khoobyarian N., Fischinger P. J. Role of heated adenovirus 2 in viral interference. Proc Soc Exp Biol Med. 1965 Nov;120(2):533–538. doi: 10.3181/00379727-120-30582. [DOI] [PubMed] [Google Scholar]
  33. Kingsbury D. W., Portner A., Darlington R. W. Properties of incomplete Sendai virions and subgenomic viral RNAs. Virology. 1970 Dec;42(4):857–871. doi: 10.1016/0042-6822(70)90335-1. [DOI] [PubMed] [Google Scholar]
  34. Kingsbury D. W., Portner A. On the genesis of incomplete Sendai virions. Virology. 1970 Dec;42(4):872–879. doi: 10.1016/0042-6822(70)90336-3. [DOI] [PubMed] [Google Scholar]
  35. LOWRY O. H., ROSEBROUGH N. J., FARR A. L., RANDALL R. J. Protein measurement with the Folin phenol reagent. J Biol Chem. 1951 Nov;193(1):265–275. [PubMed] [Google Scholar]
  36. Levine A. J., Ginsberg H. S. Mechanism by which fiber antigen inhibits multiplication of type 5 adenovirus. J Virol. 1967 Aug;1(4):747–757. doi: 10.1128/jvi.1.4.747-757.1967. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. MACPHERSON I., MONTAGNIER L. AGAR SUSPENSION CULTURE FOR THE SELECTIVE ASSAY OF CELLS TRANSFORMED BY POLYOMA VIRUS. Virology. 1964 Jun;23:291–294. doi: 10.1016/0042-6822(64)90301-0. [DOI] [PubMed] [Google Scholar]
  38. Marcus P. I., Salb J. M. Molecular basis of interferon action: inhibition of viral RNA translation. Virology. 1966 Nov;30(3):502–516. doi: 10.1016/0042-6822(66)90126-7. [DOI] [PubMed] [Google Scholar]
  39. McAuslan B. R., Smith W. R. Deoxyribonucleic acid synthesis in FV-3-infected mammalian cells. J Virol. 1968 Oct;2(10):1006–1015. doi: 10.1128/jvi.2.10.1006-1015.1968. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. McCormick W., Penman S. Replication of mengovirus in HeLa cells preinfected with nonreplicating poliovirus. J Virol. 1968 Sep;2(9):859–864. doi: 10.1128/jvi.2.9.859-864.1968. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Mekler L. B., Shlyankevich M. A., Shevliaghyn V. J. Sendai virus RNA as messenger RNA determining the synthesis of early virus specific proteins. Arch Gesamte Virusforsch. 1970;30(4):309–315. doi: 10.1007/BF01258361. [DOI] [PubMed] [Google Scholar]
  42. Moss B. Inhibition of HeLa cell protein synthesis by the vaccinia virion. J Virol. 1968 Oct;2(10):1028–1037. doi: 10.1128/jvi.2.10.1028-1037.1968. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. O'Neill F. J., Miles C. P. Virus-induced chromosome pulverization in human diploid cells. Proc Soc Exp Biol Med. 1970 Jul;134(3):825–830. doi: 10.3181/00379727-134-34892. [DOI] [PubMed] [Google Scholar]
  44. PEREIRA H. G. A virus inhibitor produced in HeLa cells infected with adenovirus. Virology. 1960 Jul;11:590–602. doi: 10.1016/0042-6822(60)90102-1. [DOI] [PubMed] [Google Scholar]
  45. POHJANPELTO P., COOPER P. D. INTERFERENCE BETWEEN POLIOVIRUSES INDUCED BY STRAINS THAT CANNOT MULTIPLY. Virology. 1965 Mar;25:350–357. doi: 10.1016/0042-6822(65)90054-1. [DOI] [PubMed] [Google Scholar]
  46. Perry J. L., To C. M., Consigli R. A. Alkaline degradation of polyoma virus. J Gen Virol. 1969 Apr;4(3):403–411. doi: 10.1099/0022-1317-4-3-403. [DOI] [PubMed] [Google Scholar]
  47. Petric M., Prevec L. Vesicular stomatitis virus--a new interfering particle, intracellular structures, and virus-specific RNA. Virology. 1970 Aug;41(4):615–630. doi: 10.1016/0042-6822(70)90427-7. [DOI] [PubMed] [Google Scholar]
  48. Portner A., Kingsbury D. W. Homologous interference by incomplete Sendai virus particles: changes in virus-specific ribonucleic acid synthesis. J Virol. 1971 Oct;8(4):388–394. doi: 10.1128/jvi.8.4.388-394.1971. [DOI] [PMC free article] [PubMed] [Google Scholar]
  49. Radloff R., Bauer W., Vinograd J. A dye-buoyant-density method for the detection and isolation of closed circular duplex DNA: the closed circular DNA in HeLa cells. Proc Natl Acad Sci U S A. 1967 May;57(5):1514–1521. doi: 10.1073/pnas.57.5.1514. [DOI] [PMC free article] [PubMed] [Google Scholar]
  50. Stampfer M., Baltimore D., Huang A. S. Ribonucleic acid synthesis of vesicular stomatitis virus. I. Species of ribonucleic acid found in Chinese hamster ovary cells infected with plaque-forming and defective particles. J Virol. 1969 Aug;4(2):154–161. doi: 10.1128/jvi.4.2.154-161.1969. [DOI] [PMC free article] [PubMed] [Google Scholar]
  51. Vilaginès R., McAuslan B. R. Interference with viral messenger RNA and DNA synthesis by superinfection with a heterologous deoxyvirus. Virology. 1970 Dec;42(4):1043–1053. doi: 10.1016/0042-6822(70)90352-1. [DOI] [PubMed] [Google Scholar]
  52. Wagner R. R., Snyder R. M., Yamazaki S. Proteins of vesicular stomatitis virus: kinetics and cellular sites of synthesis. J Virol. 1970 May;5(5):548–558. doi: 10.1128/jvi.5.5.548-558.1970. [DOI] [PMC free article] [PubMed] [Google Scholar]
  53. Wertz G. W., Youngner J. S. Inhibition of protein synthesis in L cells infected with vesicular stomatitis virus. J Virol. 1972 Jan;9(1):85–89. doi: 10.1128/jvi.9.1.85-89.1972. [DOI] [PMC free article] [PubMed] [Google Scholar]
  54. Winocour E., Robbins E. Histone synthesis in polyoma- and SV40-infected cells. Virology. 1970 Feb;40(2):307–315. doi: 10.1016/0042-6822(70)90406-x. [DOI] [PubMed] [Google Scholar]
  55. Yaoi Y., Amano M. Inhibitory effect of ultraviolet-inactivated vesicular stomatitis virus on initiation o DNA synthesis in cultured chick embryo cells. J Gen Virol. 1970 Oct;9(1):69–75. doi: 10.1099/0022-1317-9-1-69. [DOI] [PubMed] [Google Scholar]

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