Molecular Cloning of Integrated Gardner-Rasheed Feline Sarcoma Virus: Genetic Structure of Its Cell-derived Sequence Differs from That of Other Tyrosine Kinase-coding Onc Genes

Overview

Journal J Virol

Publisher American Society for Microbiology

Date 1983 Sep 1

PMID 6312085

Citations 15

Authors

G Naharro

S R Tronick

S Rasheed

M B Gardner

S A Aaronson

K C ROBBINS

Affiliations

Soon will be listed here.

Abstract

Gardner-Rasheed feline sarcoma virus (GR-FeSV) is an acute transforming retrovirus which encodes a gag-onc polyprotein possessing an associated tyrosine kinase activity. The integrated form of this virus, isolated in the Charon 21A strain of bacteriophage lambda, demonstrated an ability to transform NIH/3T3 cells at high efficiency upon transfection. Foci induced by GR-FeSV DNA contained rescuable sarcoma virus and expressed GR-P70, the major GR-FeSV translational product. The localization of long-terminal repeats within the DNA clone made it possible to establish the length of the GR-FeSV provirus as 4.6 kilobase pairs. The analysis of heteroduplexes formed between lambda feline leukemia virus (FeLV) and lambda GR-FeSV DNAs revealed the presence of a 1,700-base-pair FeLV unrelated segment, designated v-fgr, within the GR-FeSV genome. The size of this region was sufficient to encode a protein of approximately 68,000 daltons and was localized immediately downstream of the FeLV gag gene coding sequences present in GR-FeSV. Thus, it is likely that this 1.7-kilobase-pair stretch encodes the onc moiety of GR-P70. Utilizing probes representing v-fgr, we detected homologous sequences in the DNAs of diverse vertebrate species, implying that v-fgr originated from a well-conserved cellular gene. The number of cellular DNA fragments hybridized by v-fgr-derived probes indicated either that proto-fgr is distributed over a very large region of cellular DNA or represents a family of related genes. By molecular hybridization, v-fgr was not directly related to the onc genes of other known retroviruses having associated tyrosine kinase activity.

Citing Articles

Gain-of-function mutations in a member of the Src family kinases cause autoinflammatory bone disease in mice and humans.

Abe K, Cox A, Takamatsu N, Velez G, Laxer R, Tse S Proc Natl Acad Sci U S A. 2019; 116(24):11872-11877.

PMID: 31138708 PMC: 6575637. DOI: 10.1073/pnas.1819825116.

Broadening the use of antiretroviral therapy: the case for feline leukemia virus.

Greggs 3rd W, Clouser C, Patterson S, Mansky L Ther Clin Risk Manag. 2011; 7:115-22.

PMID: 21479142 PMC: 3071348. DOI: 10.2147/TCRM.S17731.

Characterization of the transforming domain of a feline sarcoma virus encoding a fgr-related tyrosine kinase.

Weyrauch G, Barnekow A Arch Virol. 1994; 134(1-2):141-55.

PMID: 8279950 DOI: 10.1007/BF01379113.

The murine c-fgr gene product associated with Ly6C and p70 integral membrane protein is expressed in cells of a monocyte/macrophage lineage.

Hatakeyama S, Iwabuchi K, Ogasawara K, GOOD R, Onoe K Proc Natl Acad Sci U S A. 1994; 91(8):3458-62.

PMID: 8159769 PMC: 43596. DOI: 10.1073/pnas.91.8.3458.

Co-transfection of normal NIH/3T3 DNA and retroval LTR sequences: a novel strategy for the detection of potential c-onc genes.

Muller R, Muller D EMBO J. 1984; 3(5):1121-7.

PMID: 6329737 PMC: 557483. DOI: 10.1002/j.1460-2075.1984.tb01939.x.

References

Aaronson S, Rowe S . Nonproducer clones of murine sarcoma virus transformed BALB-3T3 cells. Virology. 1970; 42(1):9-19. DOI: 10.1016/0042-6822(70)90233-3. View

Graham F, Van Der Eb A . A new technique for the assay of infectivity of human adenovirus 5 DNA. Virology. 1973; 52(2):456-67. DOI: 10.1016/0042-6822(73)90341-3. View

Gardner M, Officer J, Rongey R, Charman H, Hartley J, Estes J . C-type RNA tumor virus in wild house mice (Mus musculus). Bibl Haematol. 1973; 39:335-44. DOI: 10.1159/000427860. View

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

Benton W, Davis R . Screening lambdagt recombinant clones by hybridization to single plaques in situ. Science. 1977; 196(4286):180-2. DOI: 10.1126/science.322279. View

Wigler M, Silverstein S, Lee L, Pellicer A, Cheng Y, Axel R . Transfer of purified herpes virus thymidine kinase gene to cultured mouse cells. Cell. 1977; 11(1):223-32. DOI: 10.1016/0092-8674(77)90333-6. View

MOSCOVICI C, MOSCOVICI M, Jimenez H, Lai M, Hayman M, Vogt P . Continuous tissue culture cell lines derived from chemically induced tumors of Japanese quail. Cell. 1977; 11(1):95-103. DOI: 10.1016/0092-8674(77)90320-8. View

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

Sternberg N, Tiemeier D, Enquist L . In vitro packaging of a lambda Dam vector containing EcoRI DNA fragments of Escherichia coli and phage P1. Gene. 1977; 1(3-4):255-80. DOI: 10.1016/0378-1119(77)90049-x. View

10.

Jainchill J, Aaronson S, Todaro G . Murine sarcoma and leukemia viruses: assay using clonal lines of contact-inhibited mouse cells. J Virol. 1969; 4(5):549-53. PMC: 375908. DOI: 10.1128/JVI.4.5.549-553.1969. View

11.

Collett M, Erikson R . Protein kinase activity associated with the avian sarcoma virus src gene product. Proc Natl Acad Sci U S A. 1978; 75(4):2021-4. PMC: 392475. DOI: 10.1073/pnas.75.4.2021. View

12.

Levinson A, Oppermann H, LEVINTOW L, Varmus H, Bishop J . Evidence that the transforming gene of avian sarcoma virus encodes a protein kinase associated with a phosphoprotein. Cell. 1978; 15(2):561-72. DOI: 10.1016/0092-8674(78)90024-7. View

13.

Duesberg P, Vogt P . Avian acute leukemia viruses MC29 and MH2 share specific RNA sequences: evidence for a second class of transforming genes. Proc Natl Acad Sci U S A. 1979; 76(4):1633-7. PMC: 383444. DOI: 10.1073/pnas.76.4.1633. View

14.

Canaani E, Aaronson S . Restriction enzyme analysis of mouse cellular type C viral DNA: emergence of new viral sequences in spontaneous AKR/J lymphomas. Proc Natl Acad Sci U S A. 1979; 76(4):1677-81. PMC: 383453. DOI: 10.1073/pnas.76.4.1677. View

15.

Donoghue D, Sharp P, Weinberg R . Comparative study of different isolates of murine sarcoma virus. J Virol. 1979; 32(3):1015-27. PMC: 525951. DOI: 10.1128/JVI.32.3.1015-1027.1979. View

16.

Van de Ven W, Reynolds Jr F, Stephenson J . The nonstructural components of polyproteins encoded by replication-defective mammalian transforming retroviruses are phosphorylated and have associated protein kinase activity. Virology. 1980; 101(1):185-97. DOI: 10.1016/0042-6822(80)90495-x. View

17.

Nunberg J, Kaufman R, Chang A, Cohen S, Schimke R . Structure and genomic organization of the mouse dihydrofolate reductase gene. Cell. 1980; 19(2):355-64. DOI: 10.1016/0092-8674(80)90510-3. View

18.

Witte O, Dasgupta A, Baltimore D . Abelson murine leukaemia virus protein is phosphorylated in vitro to form phosphotyrosine. Nature. 1980; 283(5750):826-31. DOI: 10.1038/283826a0. View

19.

Barbacid M, Lauver A, Devare S . Biochemical and immunological characterization of polyproteins coded for by the McDonough, Gardner-Arnstein, and Snyder-Theilen strains of feline sarcoma virus. J Virol. 1980; 33(1):196-207. PMC: 288536. DOI: 10.1128/JVI.33.1.196-207.1980. View

20.

DE Wet J, Daniels D, Schroeder J, Williams B, Moore D, Blattner F . Restriction maps for twenty-one Charon vector phages. J Virol. 1980; 33(1):401-10. PMC: 288556. DOI: 10.1128/JVI.33.1.401-410.1980. View