Rearrangement of a DNA Sequence Homologous to a Cell-virus Junction Fragment in Several Moloney Murine Leukemia Virus-induced Rat Thymomas

Overview

Journal Proc Natl Acad Sci U S A

Specialty Science

Date 1984 Jan 1

PMID 6607472

Citations 42

Authors

G Lemay

P Jolicoeur

Affiliations

Soon will be listed here.

Abstract

We have studied the integrated proviruses in Moloney murine leukemia virus-induced rat thymomas. By Southern blot analysis, we found several complete integrated proviruses in each tumor. In most tumors, we could not detect defective or recombinant proviruses. Several of these integrated proviruses (with their flanking cellular sequences) from a single tumor were cloned in Charon 4A. Their flanking cellular fragments were subcloned into pBR322 and used as a probe to screen other thymoma DNAs. With one clone (pMo-lC) used as a probe, we could detect novel fragments in 11 out of 20 thymoma DNAs analyzed. In three of these thymomas we could analyze in more detail, it appears that these novel fragments are generated by the insertion of a provirus. This specific integration of Moloney provirus in the host genome may represent an important genetic event leading to tumor formation.

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References

Shoemaker C, Goff S, Gilboa E, Paskind M, Mitra S, Baltimore D . Structure of a cloned circular Moloney murine leukemia virus DNA molecule containing an inverted segment: implications for retrovirus integration. Proc Natl Acad Sci U S A. 1980; 77(7):3932-6. PMC: 349741. DOI: 10.1073/pnas.77.7.3932. View

Maniatis T, Hardison R, Lacy E, Lauer J, OConnell C, Quon D . The isolation of structural genes from libraries of eucaryotic DNA. Cell. 1978; 15(2):687-701. DOI: 10.1016/0092-8674(78)90036-3. View

Payne G, Courtneidge S, Crittenden L, Fadly A, Bishop J, Varmus H . Analysis of avian leukosis virus DNA and RNA in bursal tumours: viral gene expression is not required for maintenance of the tumor state. Cell. 1981; 23(2):311-22. DOI: 10.1016/0092-8674(81)90127-6. View

Neel B, Hayward W, Robinson H, Fang J, Astrin S . Avian leukosis virus-induced tumors have common proviral integration sites and synthesize discrete new RNAs: oncogenesis by promoter insertion. Cell. 1981; 23(2):323-34. DOI: 10.1016/0092-8674(81)90128-8. View

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

van der Putten H, Quint W, van Raaij J, Maandag E, Verma I, Berns A . M-MuLV-induced leukemogenesis: integration and structure of recombinant proviruses in tumors. Cell. 1981; 24(3):729-39. DOI: 10.1016/0092-8674(81)90099-4. View

Fung Y, Fadly A, Crittenden L, Kung H . On the mechanism of retrovirus-induced avian lymphoid leukosis: deletion and integration of the proviruses. Proc Natl Acad Sci U S A. 1981; 78(6):3418-22. PMC: 319579. DOI: 10.1073/pnas.78.6.3418. View

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

Noori-Daloii M, Swift R, Kung H, Crittenden L, Witter R . Specific integration of REV proviruses in avian bursal lymphomas. Nature. 1981; 294(5841):574-6. DOI: 10.1038/294574a0. View

10.

Payne G, Bishop J, Varmus H . Multiple arrangements of viral DNA and an activated host oncogene in bursal lymphomas. Nature. 1982; 295(5846):209-14. DOI: 10.1038/295209a0. View

11.

Robinson H, Blais B, Tsichlis P, Coffin J . At least two regions of the viral genome determine the oncogenic potential of avian leukosis viruses. Proc Natl Acad Sci U S A. 1982; 79(4):1225-9. PMC: 345934. DOI: 10.1073/pnas.79.4.1225. View

12.

Nusse R, Varmus H . Many tumors induced by the mouse mammary tumor virus contain a provirus integrated in the same region of the host genome. Cell. 1982; 31(1):99-109. DOI: 10.1016/0092-8674(82)90409-3. View

13.

Rassart E, Lemay G, DesGroseillers L, Jolicoeur P . New class of leukemogenic ecotropic recombinant murine leukemia virus isolated from radiation-induced thymomas of C57BL/6 mice. J Virol. 1983; 45(2):565-75. PMC: 256450. DOI: 10.1128/JVI.45.2.565-575.1983. View

14.

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

15.

DesGroseillers L, Villemur R, Jolicoeur P . The high leukemogenic potential of Gross passage A murine leukemia virus maps in the region of the genome corresponding to the long terminal repeat and to the 3' end of env. J Virol. 1983; 47(1):24-32. PMC: 255191. DOI: 10.1128/JVI.47.1.24-32.1983. View

16.

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; 16(4):863-74. DOI: 10.1016/0092-8674(79)90101-6. View

17.

Tsichlis P, Coffin J . Role of the C region in relative growth rates of endogenous and exogenous avian oncoviruses. Cold Spring Harb Symp Quant Biol. 1980; 44 Pt 2,:1123-32. DOI: 10.1101/sqb.1980.044.01.121. View

18.

Southern E . Detection of specific sequences among DNA fragments separated by gel electrophoresis. J Mol Biol. 1975; 98(3):503-17. DOI: 10.1016/s0022-2836(75)80083-0. View

19.

Blattner F, Williams B, Blechl A, Faber H, Furlong L, Grunwald D . Charon phages: safer derivatives of bacteriophage lambda for DNA cloning. Science. 1977; 196(4286):161-9. DOI: 10.1126/science.847462. View

20.

Rigby P, Dieckmann M, Rhodes C, Berg P . Labeling deoxyribonucleic acid to high specific activity in vitro by nick translation with DNA polymerase I. J Mol Biol. 1977; 113(1):237-51. DOI: 10.1016/0022-2836(77)90052-3. View