Sequences Responsible for Erythroid and Lymphoid Leukemia in the Long Terminal Repeats of Friend-mink Cell Focus-forming and Moloney Murine Leukemia Viruses

Overview

Journal J Virol

Publisher American Society for Microbiology

Date 1987 Jun 1

PMID 3033317

Citations 47

Authors

A Ishimoto

M Takimoto

A Adachi

M Kakuyama

S Kato

K Kakimi

K Fukuoka

T Ogiu

M Matsuyama

Affiliations

Soon will be listed here.

Abstract

Despite the high degree of homology (91%) between the nucleotide sequences of the Friend-mink cell focus-forming (MCF) and the Moloney murine leukemia virus (MuLV) genomic long terminal repeats (LTRs), the pathogenicities determined by the LTR sequences of the two viruses are quite different. Friend-MCF MuLV is an erythroid leukemia virus, and Moloney MuLV is a lymphoid leukemia virus. To map the LTR sequences responsible for the different disease specificities, we constructed nine viruses with LTRs recombinant between the Friend-MCF and Moloney MuLVs. Analysis of the leukemia induced with the recombinant viruses showed that a 195-base-pair nucleotide sequence, including a 75-base-pair nucleotide Moloney enhancer, is responsible for the tissue-specific leukemogenicity of Moloney MuLV. However, not only the enhancer but also its downstream sequences appear to be necessary. The Moloney virus enhancer and its downstream sequence exerted a dominant effect over that of the Friend-MCF virus, but the enhancer sequence alone did not. The results that three of the nine recombinant viruses induced both erythroid and lymphoid leukemias supported the hypothesis that multiple viral genetic determinants control both the ability to cause leukemia and the type of leukemia induced.

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References

Odaka T, Sugano H, Takizawa K . Inheritance of susceptibility to Friend mouse leukemia virus. 8. Effect of a single genetic locus on the pathogenesis of the leukemia. Int J Cancer. 1972; 10(2):382-90. DOI: 10.1002/ijc.2910100220. View

Todaro G, Green H . Quantitative studies of the growth of mouse embryo cells in culture and their development into established lines. J Cell Biol. 1963; 17:299-313. PMC: 2106200. DOI: 10.1083/jcb.17.2.299. View

Henderson I, Lieber M, Todaro G . Mink cell line Mv 1 Lu (CCL 64). Focus formation and the generation of "nonproducer" transformed cell lines with murine and feline sarcoma viruses. Virology. 1974; 60(1):282-7. DOI: 10.1016/0042-6822(74)90386-9. View

Hartley J, Rowe W . Clonal cells lines from a feral mouse embryo which lack host-range restrictions for murine leukemia viruses. Virology. 1975; 65(1):128-34. DOI: 10.1016/0042-6822(75)90013-6. View

Peebles P . An in vitro focus-induction assay for xenotropic murine leukemia virus, feline leukemia virus C, and the feline--primate viruses RD-114/CCC/M-7. Virology. 1975; 67(1):288-91. DOI: 10.1016/0042-6822(75)90427-4. View

Hartley J, Wolford N, Old L, Rowe W . A new class of murine leukemia virus associated with development of spontaneous lymphomas. Proc Natl Acad Sci U S A. 1977; 74(2):789-92. PMC: 392380. DOI: 10.1073/pnas.74.2.789. View

Wigler M, Pellicer A, Silverstein S, Axel R, Urlaub G, Chasin L . DNA-mediated transfer of the adenine phosphoribosyltransferase locus into mammalian cells. Proc Natl Acad Sci U S A. 1979; 76(3):1373-6. PMC: 383253. DOI: 10.1073/pnas.76.3.1373. View

Birnboim H, DOLY J . A rapid alkaline extraction procedure for screening recombinant plasmid DNA. Nucleic Acids Res. 1979; 7(6):1513-23. PMC: 342324. DOI: 10.1093/nar/7.6.1513. View

Van Beveren C, Goddard J, Berns A, Verma I . Structure of Moloney murine leukemia viral DNA: nucleotide sequence of the 5' long terminal repeat and adjacent cellular sequences. Proc Natl Acad Sci U S A. 1980; 77(6):3307-11. PMC: 349604. DOI: 10.1073/pnas.77.6.3307. View

10.

Hayward W, Neel B, Astrin S . Activation of a cellular onc gene by promoter insertion in ALV-induced lymphoid leukosis. Nature. 1981; 290(5806):475-80. DOI: 10.1038/290475a0. View

11.

Ishimoto A, Adachi A, Sakai K, Yorifuji T, Tsuruta S . Rapid emergence of mink cell focus-forming (MCF) virus in various mice infected with NB-tropic friend virus. Virology. 1981; 113(2):644-55. DOI: 10.1016/0042-6822(81)90193-8. View

12.

Shinnick T, Lerner R, Sutcliffe J . Nucleotide sequence of Moloney murine leukaemia virus. Nature. 1981; 293(5833):543-8. DOI: 10.1038/293543a0. View

13.

Van Beveren C, Rands E, Chattopadhyay S, Lowy D, Verma I . Long terminal repeat of murine retroviral DNAs: sequence analysis, host-proviral junctions, and preintegration site. J Virol. 1982; 41(2):542-56. PMC: 256783. DOI: 10.1128/JVI.41.2.542-556.1982. View

14.

Hoffmann J, Steffen D, Gusella J, Tabin C, Bird S, Cowing D . DNA methylation affecting the expression of murine leukemia proviruses. J Virol. 1982; 44(1):144-57. PMC: 256248. DOI: 10.1128/JVI.44.1.144-157.1982. View

15.

Bosselman R, van Straaten F, Van Beveren C, Verma I, Vogt M . Analysis of the env gene of a molecularly cloned and biologically active Moloney mink cell focus-forming proviral DNA. J Virol. 1982; 44(1):19-31. PMC: 256237. DOI: 10.1128/JVI.44.1.19-31.1982. View

16.

Laimins L, Khoury G, Gorman C, Howard B, Gruss P . Host-specific activation of transcription by tandem repeats from simian virus 40 and Moloney murine sarcoma virus. Proc Natl Acad Sci U S A. 1982; 79(21):6453-7. PMC: 347144. DOI: 10.1073/pnas.79.21.6453. View

17.

Tsichlis P, STRAUSS P, Hu L . A common region for proviral DNA integration in MoMuLV-induced rat thymic lymphomas. Nature. 1983; 302(5907):445-9. DOI: 10.1038/302445a0. View

18.

DesGroseillers L, Rassart E, Jolicoeur P . Thymotropism of murine leukemia virus is conferred by its long terminal repeat. Proc Natl Acad Sci U S A. 1983; 80(14):4203-7. PMC: 384005. DOI: 10.1073/pnas.80.14.4203. View

19.

Chatis P, Holland C, Hartley J, Rowe W, Hopkins N . Role for the 3' end of the genome in determining disease specificity of Friend and Moloney murine leukemia viruses. Proc Natl Acad Sci U S A. 1983; 80(14):4408-11. PMC: 384047. DOI: 10.1073/pnas.80.14.4408. View

20.

Lenz J, Celander D, Crowther R, Patarca R, Perkins D, Haseltine W . Determination of the leukaemogenicity of a murine retrovirus by sequences within the long terminal repeat. Nature. 1984; 308(5958):467-70. DOI: 10.1038/308467a0. View