Skip to main content
NCBI home page
Journal of Virology logoLink to Journal of Virology
. 1979 Dec;32(3):925–933. doi: 10.1128/jvi.32.3.925-933.1979

Conserved Region of Mammalian Retrovirus RNA

R Kominami 1, M Hatanaka 2
PMCID: PMC525941  PMID: 229272

Abstract

The viral RNAs of various mammalian retroviruses contain highly conserved sequences close to their 3′ ends. This was demonstrated by interviral molecular hybridization between fractionated viral complementary DNA (cDNA) and RNA. cDNA near the 3′ end (cDNA3′) from a rat virus (RPL strain) was fractionated by size and mixed with mouse virus RNA (Rauscher leukemia virus). No hybridization occurred with total cDNA (cDNAtotal), in agreement with previous results, but a cross-reacting sequence was found with the fractionated cDNA3′. The sequences between 50 to 400 nucleotides from the 3′ terminus of heteropolymeric RNA were most hybridizable. The rat viral cDNA3′ hybridized with mouse virus RNA more extensively than with RNA of remotely related retroviruses. The related viral sequence of the rodent viruses (mouse and rat) showed as much divergence in heteroduplex thermal denaturation profiles as did the unique sequence DNA of these two rodents. This suggests that over a period of time, rodent viruses have preserved a sequence with changes correlated to phylogenetic distance of hosts. The cross-reacting sequence of replication-competent retroviruses was conserved even in the genome of the replication-defective sarcoma virus and was also located in these genomes near the 3′ end of 30S RNA. A fraction of RD114 cDNA3′, corresponding to the conserved region, cross-hybridized extensively with RNA of a baboon endogenous virus (M7). Fractions of similar size prepared from cDNA3′ of MPMV, a primate type D virus, hybridized with M7 RNA to a lesser extent. Hybridization was not observed between Mason-Pfizer monkey virus and M7 if total cDNA's were incubated with viral RNAs. The degree of cross-reaction of the shared sequence appeared to be influenced by viral ancestral relatedness and host cell phylogenetic relationships. Thus, the strikingly high extent of cross-reaction at the conserved region between rodent viruses and simian sarcoma virus and between baboon virus and RD114 virus may reflect ancestral relatedness of the viruses. Slight cross-reaction at the site between type B and C viruses of rodents (mouse mammary tumor virus and RPL virus, 58-2T) or type C and D viruses of primates (M7, RD114, and Mason-Pfizer monkey virus) may have arisen at the conserved region through a mechanism that depends more on the phylogenetic relatedness of the host cells than on the viral type or origin. Determining the sequence of the conserved region may help elucidate this mechanism. The conserved sequences in retroviruses described here may be an important functional unit for the life cycle of many retroviruses.

Full text

PDF
925

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Aaronson S. A., Rowe S. P. Nonproducer clones of murine sarcoma virus transformed BALB-3T3 cells. Virology. 1970 Sep;42(1):9–19. doi: 10.1016/0042-6822(70)90233-3. [DOI] [PubMed] [Google Scholar]
  2. Aviv H., Leder P. Purification of biologically active globin messenger RNA by chromatography on oligothymidylic acid-cellulose. Proc Natl Acad Sci U S A. 1972 Jun;69(6):1408–1412. doi: 10.1073/pnas.69.6.1408. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Baltimore D. Tumor viruses: 1974. Cold Spring Harb Symp Quant Biol. 1975;39(Pt 2):1187–1200. doi: 10.1101/sqb.1974.039.01.137. [DOI] [PubMed] [Google Scholar]
  4. Benveniste R. E., Lieber M. M., Livingston D. M., Sherr C. J., Todaro G. J., Kalter S. S. Infectious C-type virus isolated from a baboon placenta. Nature. 1974 Mar 1;248(5443):17–20. doi: 10.1038/248017a0. [DOI] [PubMed] [Google Scholar]
  5. Benveniste R. E., Sherr C. J., Todaro G. J. Evolution of type C viral genes: origin of feline leukemia virus. Science. 1975 Nov 28;190(4217):886–888. doi: 10.1126/science.52892. [DOI] [PubMed] [Google Scholar]
  6. Benveniste R. E., Todaro G. J. Evolution of C-type viral genes: inheritance of exogenously acquired viral genes. Nature. 1974 Dec 6;252(5483):456–459. doi: 10.1038/252456a0. [DOI] [PubMed] [Google Scholar]
  7. Benveniste R. E., Todaro G. J. Evolution of type C viral genes: preservation of ancestral murine type C viral sequences in pig cellular DNA. Proc Natl Acad Sci U S A. 1975 Oct;72(10):4090–4094. doi: 10.1073/pnas.72.10.4090. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Benveniste R. E., Todaro G. J. Homology between type-C viruses of various species as determined by molecular hybridization. Proc Natl Acad Sci U S A. 1973 Dec;70(12):3316–3320. doi: 10.1073/pnas.70.12.3316. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Britten R. J., Graham D. E., Neufeld B. R. Analysis of repeating DNA sequences by reassociation. Methods Enzymol. 1974;29:363–418. doi: 10.1016/0076-6879(74)29033-5. [DOI] [PubMed] [Google Scholar]
  10. Coffin J. M., Hageman T. C., Maxam A. M., Haseltine W. A. Structure of the genome of Moloney murine leukemia virus: a terminally redundant sequence. Cell. 1978 Apr;13(4):761–773. doi: 10.1016/0092-8674(78)90226-x. [DOI] [PubMed] [Google Scholar]
  11. Fan H., Baltimore D. RNA metabolism of murine leukemia virus: detection of virus-specific RNA sequences in infected and uninfected cells and identification of virus-specific messenger RNA. J Mol Biol. 1973 Oct 15;80(1):93–117. doi: 10.1016/0022-2836(73)90235-0. [DOI] [PubMed] [Google Scholar]
  12. Friedman E. Y., Rosbash M. The syntheiss of high yields of full-length reverse transcripts of globin mRNA. Nucleic Acids Res. 1977 Oct;4(10):3455–3471. doi: 10.1093/nar/4.10.3455. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Haseltine W. A., Kleid D. G. A method for classification of 5' termini of retroviruses. Nature. 1978 Jun 1;273(5661):358–364. doi: 10.1038/273358a0. [DOI] [PubMed] [Google Scholar]
  14. Haseltine W. A., Kleid D. G., Panet A., Rothenberg E., Baltimore D. Ordered transcription of RNA tumor virus genomes. J Mol Biol. 1976 Sep 5;106(1):109–131. doi: 10.1016/0022-2836(76)90303-x. [DOI] [PubMed] [Google Scholar]
  15. Hatanaka M., Huebner R. J., Gilden R. V. Specificity of the DNA product of the C-type virus RNA-dependent DNA polymerase. Proc Natl Acad Sci U S A. 1971 Jan;68(1):10–12. doi: 10.1073/pnas.68.1.10. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Hayward W. S. Size and genetic content of viral RNAs in avian oncovirus-infected cells. J Virol. 1977 Oct;24(1):47–63. doi: 10.1128/jvi.24.1.47-63.1977. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Hu S., Davidson N. A heteroduplex study of the sequence relationships between the RNAs of M-MSV and M-MLV. Cell. 1977 Mar;10(3):469–477. doi: 10.1016/0092-8674(77)90034-4. [DOI] [PubMed] [Google Scholar]
  18. Hu S., Davidson N., Nicolson M. O., McAllister R. M. Heteroduplex study of the sequence relations between RD-114 and baboon viral RNAs. J Virol. 1977 Aug;23(2):345–352. doi: 10.1128/jvi.23.2.345-352.1977. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Huebner R. J., Hartley J. W., Rowe W. P., Lane W. T., Capps W. I. Rescue of the defective genome of Moloney sarcoma virus from a noninfectious hamster tumor and the production of pseudotype sarcoma viruses with various murine leukemia viruses. Proc Natl Acad Sci U S A. 1966 Oct;56(4):1164–1169. doi: 10.1073/pnas.56.4.1164. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Joho R. H., Billeter M. A., Weissmann C. Mapping of biological functions on RNA of avian tumor viruses: location of regions required for transformation and determination of host range. Proc Natl Acad Sci U S A. 1975 Dec;72(12):4772–4776. doi: 10.1073/pnas.72.12.4772. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Lieber M. M., Sherr C. J., Todaro G. J., Benveniste R. E., Callahan R., Coon H. G. Isolation from the asian mouse Mus caroli of an endogenous type C virus related to infectious primate type C viruses. Proc Natl Acad Sci U S A. 1975 Jun;72(6):2315–2319. doi: 10.1073/pnas.72.6.2315. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Livingston D. M., Todaro G. J. Endogenous type C virus from a cat cell clone with properties distinct from previously described feline type C virus. Virology. 1973 May;53(1):142–151. doi: 10.1016/0042-6822(73)90473-x. [DOI] [PubMed] [Google Scholar]
  23. Loening U. E. The determination of the molecular weight of ribonucleic acid by polyacrylamide-gel electrophresis. The effects of changes in conformation. Biochem J. 1969 Jun;113(1):131–138. doi: 10.1042/bj1130131. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. McAllister R. M., Nicolson M., Gardner M. B., Rongey R. W., Rasheed S., Sarma P. S., Huebner R. J., Hatanaka M., Oroszlan S., Gilden R. V. C-type virus released from cultured human rhabdomyosarcoma cells. Nat New Biol. 1972 Jan 5;235(53):3–6. doi: 10.1038/newbio235003a0. [DOI] [PubMed] [Google Scholar]
  25. Neiman P. E. Mapping by competitive hybridization of sequences which differ between endogenous and exogenous chicken leukosis viruses. Virology. 1978 Mar;85(1):9–16. doi: 10.1016/0042-6822(78)90407-5. [DOI] [PubMed] [Google Scholar]
  26. Okabe H., Gilden R. V., Hatanaka M. Extensive homology of RD114 virus DNA with RNA of feline cell origin. Nat New Biol. 1973 Jul 11;244(132):54–56. doi: 10.1038/newbio244054a0. [DOI] [PubMed] [Google Scholar]
  27. Okabe H., Gilden R. V., Hatanaka M. Specificity of the DNA product of RNA-dependent DNA polymerase in type C viruses. II. Quantitative analysis. Proc Natl Acad Sci U S A. 1973 Dec;70(12):3923–3927. doi: 10.1073/pnas.70.12.3923. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Okabe H., Gilden R. V., Hatanaka M. Specificity of the DNA product of RNA-dependent DNA polymerase in type C viruses: 3. Analysis of viruses derived from Syrian hamsters. Proc Natl Acad Sci U S A. 1974 Aug;71(8):3278–3282. doi: 10.1073/pnas.71.8.3278. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Okabe H., Gilden R. V., Hatanaka M., Stephenson J. R., Gallagher R. E., Aaronson S. A., Gallo R. C., Tronick S. R. Immunological and biochemical characterisation of type C viruses isolated from cultured human AML cells. Nature. 1976 Mar 18;260(5548):264–266. doi: 10.1038/260264a0. [DOI] [PubMed] [Google Scholar]
  30. Quintrell N., Varmus H. E., Bishop J. M., Nicholson M. O., McAllister R. M. Homologies among the nucleotide sequences of the genomes of C-type viruses. Virology. 1974 Apr;58(2):568–575. doi: 10.1016/0042-6822(74)90090-7. [DOI] [PubMed] [Google Scholar]
  31. Sanger F., Air G. M., Barrell B. G., Brown N. L., Coulson A. R., Fiddes C. A., Hutchison C. A., Slocombe P. M., Smith M. Nucleotide sequence of bacteriophage phi X174 DNA. Nature. 1977 Feb 24;265(5596):687–695. doi: 10.1038/265687a0. [DOI] [PubMed] [Google Scholar]
  32. Scolnick E. M., Parks W., Kawakami T., Kohne D., Okabe H., Gilden R., Hatanaka M. Primate and murine type-C viral nucleic acid association kinetics: analysis of model systems and natural tissues. J Virol. 1974 Feb;13(2):363–369. doi: 10.1128/jvi.13.2.363-369.1974. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Shih T. Y., Young H. A., Coffin J. M., Scolnick E. M. Physical map of the Kirsten sarcoma virus genome as determined by fingerprinting RNase T1-resistant oligonucleotides. J Virol. 1978 Jan;25(1):238–252. doi: 10.1128/jvi.25.1.238-252.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Tal J., Kung H. J., Varmus H. E., Bishop J. M. Characterization of DNA complementary to nucleotide sequences adjacent to poly(A) at the 3'-terminus of the avian sarcoma virus genome. Virology. 1977 Jun 1;79(1):183–197. doi: 10.1016/0042-6822(77)90344-0. [DOI] [PubMed] [Google Scholar]
  35. Taylor J. M., Illmensee R., Summers J. Efficeint transcription of RNA into DNA by avian sarcoma virus polymerase. Biochim Biophys Acta. 1976 Sep 6;442(3):324–330. doi: 10.1016/0005-2787(76)90307-5. [DOI] [PubMed] [Google Scholar]
  36. Todaro G. J., Benveniste R. E., Sherwin S. A., Sherr C. J. MAC-1, a new genetically transmitted type C virus of primates: "low frequency" activation from stumptail monkey cell cultures. Cell. 1978 Apr;13(4):775–782. doi: 10.1016/0092-8674(78)90227-1. [DOI] [PubMed] [Google Scholar]
  37. Tsuchida N., Gilden R. V., Hatanaka M. Sarcoma-virus-related RNA sequences in normal rat cells. Proc Natl Acad Sci U S A. 1974 Nov;71(11):4503–4507. doi: 10.1073/pnas.71.11.4503. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Tsuchida N., Long C., Hatanaka M. Viral RNA of murine sarcoma virus produced by a hamster-mouse somatic cell hybrid. Virology. 1974 Jul;60(1):200–205. doi: 10.1016/0042-6822(74)90377-8. [DOI] [PubMed] [Google Scholar]
  39. Tsuchida N., Shih M. S., Gilden R. V., Hatanaka M. Sarcoma and helper-specific RNA tumor virus subunits in transformed nonproducer mouse cells activated to produce virus by treatment with bromodeoxyuridine. J Virol. 1974 Nov;14(5):1262–1267. doi: 10.1128/jvi.14.5.1262-1267.1974. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Wang L. H., Duesberg P. H., Kawai S., Hanafusa H. Location of envelope-specific and sarcoma-specific oligonucleotides on RNA of Schmidt-Ruppin Rous sarcoma virus. Proc Natl Acad Sci U S A. 1976 Feb;73(2):447–451. doi: 10.1073/pnas.73.2.447. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Wang L. H., Duesberg P., Beemon K., Vogt P. K. Mapping RNase T1-resistant oligonucleotides of avian tumor virus RNAs: sarcoma-specific oligonucleotides are near the poly(A) end and oligonucleotides common to sarcoma and transformation-defective viruses are at the poly(A) end. J Virol. 1975 Oct;16(4):1051–1070. doi: 10.1128/jvi.16.4.1051-1070.1975. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Wang L., Galehouse D., Mellon P., Duesberg P., Mason W. S., Vogt P. K. Mapping oligonucleotides of Rous sarcoma virus RNA that segregate with polymerase and group-specific antigen markers in recombinants. Proc Natl Acad Sci U S A. 1976 Nov;73(11):3952–3956. doi: 10.1073/pnas.73.11.3952. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Weiss S. R., Varmus H. E., Bishop J. M. The size and genetic composition of virus-specific RNAs in the cytoplasm of cells producing avian sarcoma-leukosis viruses. Cell. 1977 Dec;12(4):983–992. doi: 10.1016/0092-8674(77)90163-5. [DOI] [PubMed] [Google Scholar]
  44. Wetmur J. G., Davidson N. Kinetics of renaturation of DNA. J Mol Biol. 1968 Feb 14;31(3):349–370. doi: 10.1016/0022-2836(68)90414-2. [DOI] [PubMed] [Google Scholar]

Articles from Journal of Virology are provided here courtesy of American Society for Microbiology (ASM)

RESOURCES