Abstract
Snyder-Theilen feline sarcoma virus (ST-FeSV) codes for a protein kinase with specificity for tyrosine residues (Barbacid et al., Proc. Natl. Acad. Sci. U.S.A. 77:5158-5163, 1980), properties analogous to those of the transforming gene product of Abelson murine leukemia virus (Witte et al., Nature (London) 283:826-831, 1980). In the present report, ST-FeSV was demonstrated to transform murine hematopoietic cells under in vitro assay conditions which detect lymphoid cell transformation by Abelson murine leukemia virus. Bone marrow colony formation was shown to require ST-FeSV, follow single-hit kinetics, and require the presence of mercaptoethanol in the agar medium. ST-FeSV-induced colonies could be established in culture as continuous cell lines that demonstrated unrestricted self-renewal capacity and leukemogenicity in vivo. The hematopoietic blast cells transformed by ST-FeSV in culture appeared to be at an early stage of B cell differentiation. They possessed Lyb 2 surface antigens, were dependent on mercaptoethanol for growth, and contained only low levels of terminal deoxynucleotidyl transferase. Moreover, a large fraction of the lines synthesized immunoglobulin mu chain in the absence of light chains. Thus, the phenotype of ST-FeSV hematopoietic transformants was indistinguishable from that of the pre-B lymphoblast transformants induced by Abelson murine leukemia virus. These findings indicate that the in vitro functional similarities in the onc gene products of ST-FeSV and Abelson murine leukemia virus may reflect a common pathway by which they exert their oncogenic potential.
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- Abelson H. T., Rabstein L. S. Lymphosarcoma: virus-induced thymic-independent disease in mice. Cancer Res. 1970 Aug;30(8):2213–2222. [PubMed] [Google Scholar]
- Andersen P. R., Devare S. G., Tronick S. R., Ellis R. W., Aaronson S. A., Scolnick E. M. Generation of BALB-MuSV and Ha-MuSC by type C virus transduction of homologous transforming genes from different species. Cell. 1981 Oct;26(1 Pt 1):129–134. doi: 10.1016/0092-8674(81)90041-6. [DOI] [PubMed] [Google Scholar]
- Barbacid M., Beemon K., Devare S. G. Origin and functional properties of the major gene product of the Snyder-Theilen strain of feline sarcoma virus. Proc Natl Acad Sci U S A. 1980 Sep;77(9):5158–5162. doi: 10.1073/pnas.77.9.5158. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Barbacid M., Breitman M. L., Lauver A. V., Long L. K., Vogt P. K. The transformation-specific proteins of avian (Fujinami and PRC-II) and feline (Synder--Theilen and Gardner--Arnstein) sarcoma viruses are immunologically related. Virology. 1981 Apr 30;110(2):411–419. doi: 10.1016/0042-6822(81)90071-4. [DOI] [PubMed] [Google Scholar]
- Barton R., Goldschneider I., Bollum F. J. The distribution of terminal deoxynucleotidyl transferase (TdT) among subsets of thymocytes in the rat. J Immunol. 1976 Feb;116(2):462–468. [PubMed] [Google Scholar]
- Beemon K. Transforming proteins of some feline and avian sarcoma viruses are related structurally and functionally. Cell. 1981 Apr;24(1):145–153. doi: 10.1016/0092-8674(81)90510-9. [DOI] [PubMed] [Google Scholar]
- Bishop J. M. Enemies within: the genesis of retrovirus oncogenes. Cell. 1981 Jan;23(1):5–6. doi: 10.1016/0092-8674(81)90263-4. [DOI] [PubMed] [Google Scholar]
- Bishop J. M. Retroviruses. Annu Rev Biochem. 1978;47:35–88. doi: 10.1146/annurev.bi.47.070178.000343. [DOI] [PubMed] [Google Scholar]
- Boss M., Greaves M., Teich N. Abelson virus-transformed haematopoietic cell lines with pre-B-cell characteristics. Nature. 1979 Apr 5;278(5704):551–553. doi: 10.1038/278551a0. [DOI] [PubMed] [Google Scholar]
- Broome J. D., Jeng M. W. Growth stimulation of mouse leukemia cells by thiols and disulfides in vitro. J Natl Cancer Inst. 1972 Aug;49(2):579–581. [PubMed] [Google Scholar]
- Chen C., Hirsch J. G. Restoration of antibody-forming capacity in cultures of nonadherent spleen cells by mercaptoethanol. Science. 1972 Apr 7;176(4030):60–61. doi: 10.1126/science.176.4030.60. [DOI] [PubMed] [Google Scholar]
- Collett M. S., Erikson R. L. Protein kinase activity associated with the avian sarcoma virus src gene product. Proc Natl Acad Sci U S A. 1978 Apr;75(4):2021–2024. doi: 10.1073/pnas.75.4.2021. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Donoghue D. J., Sharp P. A., Weinberg R. A. Comparative study of different isolates of murine sarcoma virus. J Virol. 1979 Dec;32(3):1015–1027. doi: 10.1128/jvi.32.3.1015-1027.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Duesberg P. H., Vogt P. K. 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 Apr;76(4):1633–1637. doi: 10.1073/pnas.76.4.1633. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Ellis R. W., Defeo D., Shih T. Y., Gonda M. A., Young H. A., Tsuchida N., Lowy D. R., Scolnick E. M. The p21 src genes of Harvey and Kirsten sarcoma viruses originate from divergent members of a family of normal vertebrate genes. Nature. 1981 Aug 6;292(5823):506–511. doi: 10.1038/292506a0. [DOI] [PubMed] [Google Scholar]
- Feldman R. A., Hanafusa T., Hanafusa H. Characterization of protein kinase activity associated with the transforming gene product of Fujinami sarcoma virus. Cell. 1980 Dec;22(3):757–765. doi: 10.1016/0092-8674(80)90552-8. [DOI] [PubMed] [Google Scholar]
- Frankel A. E., Gilbert J. H., Porzig K. J., Scolnick E. M., Aaronson S. A. Nature and distribution of feline sarcoma virus nucleotide sequences. J Virol. 1979 Jun;30(3):821–827. doi: 10.1128/jvi.30.3.821-827.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Ghysdael J., Neil J. C., Vogt P. K. A third class of avian sarcoma viruses, defined by related transformation-specific proteins of Yamaguchi 73 and Esh sarcoma viruses. Proc Natl Acad Sci U S A. 1981 Apr;78(4):2611–2615. doi: 10.1073/pnas.78.4.2611. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Graf T., Beug H. Avian leukemia viruses: interaction with their target cells in vivo and in vitro. Biochim Biophys Acta. 1978 Nov 17;516(3):269–299. doi: 10.1016/0304-419x(78)90011-2. [DOI] [PubMed] [Google Scholar]
- Hampe A., Laprevotte I., Galibert F., Fedele L. A., Sherr C. J. Nucleotide sequences of feline retroviral oncogenes (v-fes) provide evidence for a family of tyrosine-specific protein kinase genes. Cell. 1982 Oct;30(3):775–785. doi: 10.1016/0092-8674(82)90282-3. [DOI] [PubMed] [Google Scholar]
- Hanafusa T., Wang L. H., Anderson S. M., Karess R. E., Hayward W. S., Hanafusa H. Characterization of the transforming gene of Fujinami sarcoma virus. Proc Natl Acad Sci U S A. 1980 May;77(5):3009–3013. doi: 10.1073/pnas.77.5.3009. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hankins W. D., Scolnick E. M. Harvey and Kirsten sarcoma viruses promote the growth and differentiation of erythroid precursor cells in vitro. Cell. 1981 Oct;26(1 Pt 1):91–97. doi: 10.1016/0092-8674(81)90036-2. [DOI] [PubMed] [Google Scholar]
- Hartley J. W., Rowe W. P. Naturally occurring murine leukemia viruses in wild mice: characterization of a new "amphotropic" class. J Virol. 1976 Jul;19(1):19–25. doi: 10.1128/jvi.19.1.19-25.1976. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Henderson I. C., Lieber M. M., Todaro G. J. 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 Jul;60(1):282–287. doi: 10.1016/0042-6822(74)90386-9. [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]
- Kawai S., Yoshida M., Segawa K., Sugiyama H., Ishizaki R., Toyoshima K. Characterization of Y73, an avian sarcoma virus: a unique transforming gene and its product, a phosphopolyprotein with protein kinase activity. Proc Natl Acad Sci U S A. 1980 Oct;77(10):6199–6203. doi: 10.1073/pnas.77.10.6199. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kerbel R. S., Davies A. J. The possible biological significance of Fc receptors on mammalian lymphocytes and tumor cells. Cell. 1974 Oct;3(2):105–112. doi: 10.1016/0092-8674(74)90113-5. [DOI] [PubMed] [Google Scholar]
- Kerbel R. S., Pross H. F., Elliott E. V. Origin and partial characterization of Fc receptor-bearing cells found within experimental carcinomas and sarcomas. Int J Cancer. 1975 Jun 15;15(6):918–932. doi: 10.1002/ijc.2910150607. [DOI] [PubMed] [Google Scholar]
- Kitamura N., Kitamura A., Toyoshima K., Hirayama Y., Yoshida M. Avian sarcoma virus Y73 genome sequence and structural similarity of its transforming gene product to that of Rous sarcoma virus. Nature. 1982 May 20;297(5863):205–208. doi: 10.1038/297205a0. [DOI] [PubMed] [Google Scholar]
- Koury M. J., Pragnell I. B. Retroviruses induce granulocyte-macrophage colony stimulating activity in fibroblasts. Nature. 1982 Oct 14;299(5884):638–640. doi: 10.1038/299638a0. [DOI] [PubMed] [Google Scholar]
- Kung P. C., Siverstone A. E., McCaffrey R. P., Baltimore D. Murine terminal deoxynucleotidyl transferase: cellular distribution and response to cortisone. J Exp Med. 1975 Apr 1;141(4):855–865. [PMC free article] [PubMed] [Google Scholar]
- Levinson A. D., Oppermann H., Levintow L., Varmus H. E., Bishop J. M. Evidence that the transforming gene of avian sarcoma virus encodes a protein kinase associated with a phosphoprotein. Cell. 1978 Oct;15(2):561–572. doi: 10.1016/0092-8674(78)90024-7. [DOI] [PubMed] [Google Scholar]
- Metcalf D., Warner N. L., Nossal G. J., Miller J. F., Shortman K., Rabellino E. Growth of B lymphocyte colonies in vitro from mouse lymphoid organs. Nature. 1975 Jun 19;255(5510):630–632. doi: 10.1038/255630a0. [DOI] [PubMed] [Google Scholar]
- Omer C. A., Faras A. J. Mechanism of release of the avian rotavirus tRNATrp primer molecule from viral DNA by ribonuclease H during reverse transcription. Cell. 1982 Oct;30(3):797–805. doi: 10.1016/0092-8674(82)90284-7. [DOI] [PubMed] [Google Scholar]
- Pawson T., Guyden J., Kung T. H., Radke K., Gilmore T., Martin G. S. A strain of Fujinami sarcoma virus which is temperature-sensitive in protein phosphorylation and cellular transformation. Cell. 1980 Dec;22(3):767–775. doi: 10.1016/0092-8674(80)90553-x. [DOI] [PubMed] [Google Scholar]
- Pierce J. H., Aaronson S. A. BALB- and Harvey-murine sarcoma virus transformation of a novel lymphoid progenitor cell. J Exp Med. 1982 Sep 1;156(3):873–887. doi: 10.1084/jem.156.3.873. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Porzig K. J., Barbacid M., Aaronson S. A. Biological properties and translational products of three independent isolates of feline sarcoma virus. Virology. 1979 Jan 15;92(1):91–107. doi: 10.1016/0042-6822(79)90217-4. [DOI] [PubMed] [Google Scholar]
- Rasheed S., Gardner M. B., Chan E. Amphotropic host range of naturally occuring wild mouse leukemia viruses. J Virol. 1976 Jul;19(1):13–18. doi: 10.1128/jvi.19.1.13-18.1976. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Reddy E. P., Dunn C. Y., Aaronson S. A. Different lymphoid cell targets by transformation by replication-competent Moloney and Rauscher mouse leukemia viruses. Cell. 1980 Mar;19(3):663–669. doi: 10.1016/s0092-8674(80)80043-2. [DOI] [PubMed] [Google Scholar]
- Rosenberg N., Baltimore D. A quantitative assay for transformation of bone marrow cells by Abelson murine leukemia virus. J Exp Med. 1976 Jun 1;143(6):1453–1463. doi: 10.1084/jem.143.6.1453. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Rosenberg N., Baltimore D., Scher C. D. In vitro transformation of lymphoid cells by Abelson murine leukemia virus. Proc Natl Acad Sci U S A. 1975 May;72(5):1932–1936. doi: 10.1073/pnas.72.5.1932. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Scher C. D., Siegler R. Direct transformation of 3T3 cells by Abelson murine leukaemia virus. Nature. 1975 Feb 27;253(5494):729–731. doi: 10.1038/253729a0. [DOI] [PubMed] [Google Scholar]
- Shibuya M., Hanafusa T., Hanafusa H., Stephenson J. R. Homology exists among the transforming sequences of avian and feline sarcoma viruses. Proc Natl Acad Sci U S A. 1980 Nov;77(11):6536–6540. doi: 10.1073/pnas.77.11.6536. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Siden E. J., Baltimore D., Clark D., Rosenberg N. E. Immunoglobulin synthesis by lymphoid cells transformed in vitro by Abelson murine leukemia virus. Cell. 1979 Feb;16(2):389–396. doi: 10.1016/0092-8674(79)90014-x. [DOI] [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]
- Van Beveren C., Galleshaw J. A., Jonas V., Berns A. J., Doolittle R. F., Donoghue D. J., Verma I. M. Nucleotide sequence and formation of the transforming gene of a mouse sarcoma virus. Nature. 1981 Jan 22;289(5795):258–262. doi: 10.1038/289258a0. [DOI] [PubMed] [Google Scholar]
- Van de Ven W. J., Reynolds F. H., Jr, Stephenson J. R. The nonstructural components of polyproteins encoded by replication-defective mammalian transforming retroviruses are phosphorylated and have associated protein kinase activity. Virology. 1980 Feb;101(1):185–197. doi: 10.1016/0042-6822(80)90495-x. [DOI] [PubMed] [Google Scholar]
- Waneck G. L., Rosenberg N. Abelson leukemia virus induces lymphoid and erythroid colonies in infected fetal cell cultures. Cell. 1981 Oct;26(1 Pt 1):79–89. doi: 10.1016/0092-8674(81)90035-0. [DOI] [PubMed] [Google Scholar]
- Witte O. N., Dasgupta A., Baltimore D. Abelson murine leukaemia virus protein is phosphorylated in vitro to form phosphotyrosine. Nature. 1980 Feb 28;283(5750):826–831. doi: 10.1038/283826a0. [DOI] [PubMed] [Google Scholar]