Dual evolutionary origin for the rat genetic sequences of Harvey murine sarcoma virus (original) (raw)
Abstract
Detailed restriction endonuclease maps were developed for Harvey murine sarcoma virus (Ha-MuSV) DNA (clone H-1), molecularly closed at its unique EcoRI site in pBR322, for three nonoverlapping subgenomic HindIII clones which together span the entire H-1 clone and for a molecularly cloned DNA copy of a portion of rat 30S RNA (which represents the majority of the rat genetic sequences in Ha-MuSV). Molecular hybridization of the 30S clone to small restriction fragments of clone H-1 revealed a 0.9-to-1.0-kilobase pair region in the 5' half of the Ha-MuSV genome not homologous to the 30S clone, although the 30S clone did contain related sequences in Ha-MuSV on both sides of this nonhomologous region. By using cloned sequences from a segment of the Ha-MuSV nonhomology region as a probe for hybridization to Southern blots of DNA from rat, mouse, bat, and chicken cells, one to three bands were detected in DNA of each species. By contrast, the 30S clone DNA was highly related to many sequences in rat DNA, partially related to fewer mouse DNA sequences, and homologous only to one to three bands in bat and chicken DNA. Earlier work had shown that the 5' half of the Ha-MuSV genome coded for transformation and for the viral p21 protein (Chang et al., J. Virol. 35: 76--92, 1980; Wei et al., Proc. Natl. Acad. Sci. U.S.A., in press). We used two subgenomic HindIII clones whose shared HindIII site mapped within the 5' region of clone H-1 nonhomologous to the 30S clone to test whether the nonhomologous segment might encode the transforming and p21 functions. Although neither of the subgenomic HindIII fragments by themselves induced transformation, ligation of these two nontransforming DNAs to each other did restore p21-mediated transformation. A conclusion consistent with these results is that a region in the 5' half of the Ha-MuSV genome evolutionarily distinct from and not present in rat 30S RNA is essential for transformation and for p21 encoding.
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- Barbacid M., Hunter E., Aaronson S. A. Avian reticuloendotheliosis viruses: evolutionary linkage with mammalian type C retroviruses. J Virol. 1979 May;30(2):508–514. doi: 10.1128/jvi.30.2.508-514.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Chang E. H., Maryak J. M., Wei C. M., Shih T. Y., Shober R., Cheung H. L., Ellis R. W., Hager G. L., Scolnick E. M., Lowy D. R. Functional organization of the Harvey murine sarcoma virus genome. J Virol. 1980 Jul;35(1):76–92. doi: 10.1128/jvi.35.1.76-92.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Chang H. W., Garon C. F., Chang E. H., Lowy D. R., Hager G. L., Scolnick E. M., Repaske R., Martin M. A. Molecular cloning of the Harvey sarcoma virus circular DNA intermediates. II. Further structural analyses. J Virol. 1980 Feb;33(2):845–855. doi: 10.1128/jvi.33.2.845-855.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Chien U. H., Lai M., Shih T. Y., Verma I. M., Scolnick E. M., Roy-Burman P., Davidson N. Heteroduplex analysis of the sequence relationships between the genomes of Kirsten and Harvey sarcoma viruses, their respective parental murine leukemia viruses, and the rat endogenous 30S RNA. J Virol. 1979 Sep;31(3):752–760. doi: 10.1128/jvi.31.3.752-760.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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]
- Colman A., Byers M. J., Primrose S. B., Lyons A. Rapid purification of plasmid DNAs by hydroxyapatite chromatography. Eur J Biochem. 1978 Nov 2;91(1):303–310. doi: 10.1111/j.1432-1033.1978.tb20966.x. [DOI] [PubMed] [Google Scholar]
- Frankel A. E., Neubauer R. L., Fischinger P. J. Fractionation of DNA nucleotide transcripts from Moloney sarcoma virus and isolation of sarcoma virus-specific complementary DNA. J Virol. 1976 May;18(2):481–490. doi: 10.1128/jvi.18.2.481-490.1976. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Gilboa E., Goff S., Shields A., Yoshimura F., Mitra S., Baltimore D. In vitro synthesis of a 9 kbp terminally redundant DNA carrying the infectivity of Moloney murine leukemia virus. Cell. 1979 Apr;16(4):863–874. doi: 10.1016/0092-8674(79)90101-6. [DOI] [PubMed] [Google Scholar]
- Graham F. L., van der Eb A. J. A new technique for the assay of infectivity of human adenovirus 5 DNA. Virology. 1973 Apr;52(2):456–467. doi: 10.1016/0042-6822(73)90341-3. [DOI] [PubMed] [Google Scholar]
- Gross-Bellard M., Oudet P., Chambon P. Isolation of high-molecular-weight DNA from mammalian cells. Eur J Biochem. 1973 Jul 2;36(1):32–38. doi: 10.1111/j.1432-1033.1973.tb02881.x. [DOI] [PubMed] [Google Scholar]
- HARVEY J. J. AN UNIDENTIFIED VIRUS WHICH CAUSES THE RAPID PRODUCTION OF TUMOURS IN MICE. Nature. 1964 Dec 12;204:1104–1105. doi: 10.1038/2041104b0. [DOI] [PubMed] [Google Scholar]
- Hager G. L., Chang E. H., Chan H. W., Garon C. F., Israel M. A., Martin M. A., Scolnick E. M., Lowy D. R. Molecular cloning of the Harvey sarcoma virus closed circular DNA intermediates: initial structural and biological characterization. J Virol. 1979 Sep;31(3):795–809. doi: 10.1128/jvi.31.3.795-809.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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]
- Hughes S. H., Payvar F., Spector D., Schimke R. T., Robinson H. L., Payne G. S., Bishop J. M., Varmus H. E. Heterogeneity of genetic loci in chickens: analysis of endogenous viral and nonviral genes by cleavage of DNA with restriction endonucleases. Cell. 1979 Oct;18(2):347–359. doi: 10.1016/0092-8674(79)90054-0. [DOI] [PubMed] [Google Scholar]
- Jainchill J. L., Aaronson S. A., Todaro G. J. Murine sarcoma and leukemia viruses: assay using clonal lines of contact-inhibited mouse cells. J Virol. 1969 Nov;4(5):549–553. doi: 10.1128/jvi.4.5.549-553.1969. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Leder P., Tiemeier D., Enquist L. EK2 derivatives of bacteriophage lambda useful in the cloning of DNA from higher organisms: the lambdagtWES system. Science. 1977 Apr 8;196(4286):175–177. doi: 10.1126/science.322278. [DOI] [PubMed] [Google Scholar]
- Lowy D. R., Rands E., Scolnick E. M. Helper-independent transformation by unintegrated Harvey sarcoma virus DNA. J Virol. 1978 May;26(2):291–298. doi: 10.1128/jvi.26.2.291-298.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
- McDonell M. W., Simon M. N., Studier F. W. Analysis of restriction fragments of T7 DNA and determination of molecular weights by electrophoresis in neutral and alkaline gels. J Mol Biol. 1977 Feb 15;110(1):119–146. doi: 10.1016/s0022-2836(77)80102-2. [DOI] [PubMed] [Google Scholar]
- Oskarsson M., McClements W. L., Blair D. G., Maizel J. V., Vande Woude G. F. Properties of a normal mouse cell DNA sequence (sarc) homologous to the src sequence of Moloney sarcoma virus. Science. 1980 Mar 14;207(4436):1222–1224. doi: 10.1126/science.6243788. [DOI] [PubMed] [Google Scholar]
- Rasheed S., Gardner M. B., Huebner R. J. In vitro isolation of stable rat sarcoma viruses. Proc Natl Acad Sci U S A. 1978 Jun;75(6):2972–2976. doi: 10.1073/pnas.75.6.2972. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Rasheed S., Young H., Gardner M. B. Inhibition of spontaneous transformation of rat embryo cells releasing endogenous type C virus by virus-specific antiserum. J Natl Cancer Inst. 1979 Sep;63(3):745–750. doi: 10.1093/jnci/63.3.745. [DOI] [PubMed] [Google Scholar]
- Roussel M., Saule S., Lagrou C., Rommens C., Beug H., Graf T., Stehelin D. Three new types of viral oncogene of cellular origin specific for haematopoietic cell transformation. Nature. 1979 Oct 11;281(5731):452–455. doi: 10.1038/281452a0. [DOI] [PubMed] [Google Scholar]
- Scolnick E. M., Howk R. S., Anisowicz A., Peebles P. T., Scher C. D., Parks W. P. Separation of sarcoma virus-specific and leukemia virus-specific genetic sequences of Moloney sarcoma virus. Proc Natl Acad Sci U S A. 1975 Nov;72(11):4650–4654. doi: 10.1073/pnas.72.11.4650. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Scolnick E. M., Papageorge A. G., Shih T. Y. Guanine nucleotide-binding activity as an assay for src protein of rat-derived murine sarcoma viruses. Proc Natl Acad Sci U S A. 1979 Oct;76(10):5355–5359. doi: 10.1073/pnas.76.10.5355. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Scolnick E. M., Parks W. P. Harvey sarcoma virus: a second murine type C sarcoma virus with rat genetic information. J Virol. 1974 Jun;13(6):1211–1219. doi: 10.1128/jvi.13.6.1211-1219.1974. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Scolnick E. M., Vass W. C., Howk R. S., Duesberg P. H. Defective retrovirus-like 30S RNA species of rat and mouse cells are infectious if packaged by type C helper virus. J Virol. 1979 Mar;29(3):964–972. doi: 10.1128/jvi.29.3.964-972.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Sharp P. A., Sugden B., Sambrook J. Detection of two restriction endonuclease activities in Haemophilus parainfluenzae using analytical agarose--ethidium bromide electrophoresis. Biochemistry. 1973 Jul 31;12(16):3055–3063. doi: 10.1021/bi00740a018. [DOI] [PubMed] [Google Scholar]
- Sherr C. J., Fedele L. A., Donner L., Turek L. P. Restriction endonuclease mapping of unintegrated proviral DNA of Snyder-Theilen feline sarcoma virus: localization of sarcoma-specific sequences. J Virol. 1979 Dec;32(3):860–875. doi: 10.1128/jvi.32.3.860-875.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Shih T. Y., Weeks M. O., Young H. A., Scholnick E. M. Identification of a sarcoma virus-coded phosphoprotein in nonproducer cells transformed by Kirsten or Harvey murine sarcoma virus. Virology. 1979 Jul 15;96(1):64–79. doi: 10.1016/0042-6822(79)90173-9. [DOI] [PubMed] [Google Scholar]
- Shih T. Y., Weeks M. O., Young H. A., Scolnick E. M. p21 of Kirsten murine sarcoma virus is thermolabile in a viral mutant temperature sensitive for the maintenance of transformation. J Virol. 1979 Aug;31(2):546–546. doi: 10.1128/jvi.31.2.546-546.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Shih T. Y., Williams D. R., Weeks M. O., Maryak J. M., Vass W. C., Scolnick E. M. Comparison of the genomic organization of Kirsten and Harvey sarcoma viruses. J Virol. 1978 Jul;27(1):45–55. doi: 10.1128/jvi.27.1.45-55.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Southern E. M. Detection of specific sequences among DNA fragments separated by gel electrophoresis. J Mol Biol. 1975 Nov 5;98(3):503–517. doi: 10.1016/s0022-2836(75)80083-0. [DOI] [PubMed] [Google Scholar]
- Spector D. H., Varmus H. E., Bishop J. M. Nucleotide sequences related to the transforming gene of avian sarcoma virus are present in DNA of uninfected vertebrates. Proc Natl Acad Sci U S A. 1978 Sep;75(9):4102–4106. doi: 10.1073/pnas.75.9.4102. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Stehelin D., Guntaka R. V., Varmus H. E., Bishop J. M. Purification of DNA complementary to nucleotide sequences required for neoplastic transformation of fibroblasts by avian sarcoma viruses. J Mol Biol. 1976 Mar 5;101(3):349–365. doi: 10.1016/0022-2836(76)90152-2. [DOI] [PubMed] [Google Scholar]
- Tronick S. R., Robbins K. C., Canaani E., Devare S. G., Andersen P. R., Aaronson S. A. Molecular cloning of Moloney murine sarcoma virus: arrangement of virus-related sequences within the normal mouse genome. Proc Natl Acad Sci U S A. 1979 Dec;76(12):6314–6318. doi: 10.1073/pnas.76.12.6314. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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]
- 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]
- Young H. A., Shih T. Y., Scolnick E. M., Rasheed S., Gardner M. B. Different rat-derived transforming retroviruses code for an immunologically related intracellular phosphoprotein. Proc Natl Acad Sci U S A. 1979 Jul;76(7):3523–3527. doi: 10.1073/pnas.76.7.3523. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Young H. A., Wenk M. L., Goodman D. G., Scolnick E. M. Expression of RNA of an endogenous replication-defective retrovirus in rat mammary adenocarcinomas induced by 7,12-dimethylbenz[a]anthracene. J Natl Cancer Inst. 1978 Nov;61(5):1329–1337. doi: 10.1093/jnci/61.5.1329. [DOI] [PubMed] [Google Scholar]