Summary
Retroviral endogenous sequences related to the envelope (env) gene of Friend spleen focus forming virus (SFFV) and of mink cell focus forming viruses (MCF) are present in the genome of various mouse strains. We have examined the transcription of these SFFV/MCF-related sequences in normal tissues of two mouse strains, ICFW and DBA/2. Cytoplasmic Poly A+ RNAs of normal mouse tissues were analyzed by dot-blot and Northern blot hybridizations with a subcloned env SFFV DNA fragment (0.4 kbp BamHI-SmaI). In both mice, the level of SFFV/MCF env related transcripts was very low in bone marrows and spleens whereas it was high in kidneys. Intermediate levels of transcripts were observed in other tissues (thymus, liver and brain). In both mouse strains, the size of SFFV/MCF env related transcripts varied from one tissue to another. Some transcripts in DBA/2 mice were reminiscent of full-size viral message indicating an occasional expression of xenotropic/MCF endogenous virus in this low-leukemic strain. Sizes of the other SFFV/MCF related env transcripts were unusual, but were similar in both strains for each tissue studied. This last result suggests a tissue-specific transcription of endogenous sequences related to the SFFV/MCF env gene. A 1.8 kb SFFV/MCF env RNA was the major transcript in the tissues which expressed a high level of these env transcripts. Treatment of mice with phenylhydrazine which greatly stimulates erythroid differentiation in spleens increased the level of SFFV/MCF related env RNAs only in the spleens, suggesting a possible correlation between the SFFV/MCF env transcription and the stimulation of the erythroid spleen cells.
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Adachi, A., Sakai, K., Kitamura, N., Nakanishi, S., Nina, O., Matsuyama, M., Ishimoto, A.: Characterization of the env gene and long terminal repeat of molecularly cloned Friend mink cell focus-inducing virus DNA. J. Virol.50, 813–821 (1984).
Amanuma, H., Katori, A., Obata, M., Sagata, N., Ikawa, Y.: Complete nucleotide sequence of the gene for the specific glycoprotein (gp 55) of Friend spleen focus forming virus. Proc. Natl. Acad. Sci. U.S.A.80, 3913–3917 (1983).
Bernstein, A., Gamble, C., Penrose, D., Mak, T. W.: Presence and expression of Friend erythroleukemia virus-related sequences in normal and leukemic mouse tissues. Proc. Natl. Acad. Sci. U.S.A.76, 4455–4459 (1979).
Blatt, C., Mileham, K., Haas, M., Nesbitt, M. N., Harper, M. E., Simon, M. I.: Chromosomal mapping of the mink cell focus-inducing and xenotropic env gene family in the mouse. Proc. Natl. Acad. Sci. U.S.A.80, 6298–6302 (1983).
Boccara, M., Souyri, M., Magarian, C., Stavnezer, E., Fleissner, E.: Evidence for a new form of retroviral env transcript in leukemic and normal mouse lymphoid cells. J. Virol.48, 102–109 (1983).
Bosselman, R. A., van Straaten, F., van Beveren, C., Verma, I. M., Vogt, M.: Analysis of the env gene of a molecularly cloned and biologically active Moloney mink cell focus-forming proviral DNA. J. Virol.44, 19–31 (1982).
Chattopadhyay, S. K., Cloyd, M. W., Linemeyer, D. L., Lander, M. R., Rands, E., Lowy, D. R.: Cellular origin and role of mink cell focus-forming viruses in murine thymic lymphomas. Nature (London)295, 25–31 (1982).
Clark, S. P., Mak, T. W.: Fluidity of a retrovirus genome. J. Virol.50, 759–765 (1984).
Coffin, J.: Endogenous viruses. In:Weiss, R., Teich, N., Varmus, H., Coffin, J. (eds.): RNA tumor viruses. Molecular Biology of Tumor Viruses, Second edition, 1109–1203. Cold Spring Harbor, N. Y.: Cold Spring Harbor Laboratory publications 1982.
Conklin, K. F., Coffin, J. M., Robinson, H. L., Groudine, M., Eisenman, R.: Role of methylation in the induced and spontaneous expression of the avian endogenous virus ev-1: DNA structure and gene products. Mol. Cell. Biol.2, 638–652 (1982).
Evans, L. H., Cloyd, M. W.: Generation of mink cell focus-forming viruses by Friend murine leukemia virus: recombination with specific endogenous proviral sequences. J. Virol.49, 772–781 (1984).
Khan, A. S., Rowe, W. P., Martin, M. A.: Cloning of endogenous murine leukemia virus-related sequences from chromosomal DNA of Balb/c and AKR/J mice: identification of an env progenitor of AKR-247 mink cell focus-forming proviral DNA. J. Virol.44, 625–636 (1982).
Khan, A. S.: Nucleotide sequence analysis establishes the role of endogenous murine leukemia virus DNA segments in formation of recombinant mink cell focus-forming murine leukemia viruses. J. Virol.50, 864–871 (1984).
Klenner, D., Horak, I., Schimpl, A., Wecker, E.: Expression of endogenous retroviral glycoprotein 70 by antigen-activated cytotoxic and suppressor T lymphocytes of mice. Proc. Natl. Acad. Sci. U.S.A.79, 1250–1253 (1982).
Krystal, G.: A simple microassay for erythropoietin based on 3 H-thymydine incorporation into spleen cells from phenylhydrazine treated mice. Exp. Hematol.11, 649–660 (1983).
Lee, E. J., Kaminchik, J., Hankins, W. D.: Expression of xenotropic-like env RNA sequences in normal DBA/2 and NZB mouse tissues. J. Virol.51, 247–250 (1984).
Levy, D. E., Lerner, R. A., Wilson, M. C.: A genetic locus regulates the expression of tissue-specific mRNAs from multiple transcription units. Proc. Natl. Acad. Sci. U.S.A.79, 5823–5827 (1982).
Mak, T. W., Axelrad, A. A., Bernstein, A.: Fv-2 locus controls expression of Friend spleen focus-forming virus-specific sequences in normal and infected mice. Proc. Natl. Acad. Sci. U.S.A.76, 5809–5812 (1979).
Mathieu-Mahul, D., Robert, J., Gisselbrecht, S., Barque, J. P., Larsen, C. J.: Analysis of viral RNA and proteins expressed by a non producer Friend erythroleukemia cell line (HFL/b cell line). Leukemia Res.5, 399–411 (1981).
Meruelo, D., Rossomando, A., Offer, M., Buxbaum, J., Pellicer, A.: Association of endogenous viral loci with genes encoding murine histocompatibility and lymphocyte differenciation antigens. Proc. Natl. Acad. Sci. U.S.A.80, 5032–5036 (1983).
Moreau-Gachelin, F., Robert-Lezenes, J., Mathieu-Mahul, D., Gisselbrecht, S., Larsen, C. J.: Isolation and characterization of a gp 70+ non producer Friend tumor cell clone. Biochimie65, 259–266 (1983).
Moreau-Gachelin, F., Robert-Lezenes, J., Wendling, F., Tavitian, A., Tambourin, P.: Integration of spleen focus-forming virus proviruses in Friend tumor cells. J. Virol.53, 292–295 (1985).
Oliff, A., Collins, L., Mirenda, C.: Molecular cloning of Friend mink cell focusinducing virus: identification of mink cell focus-inducing virus-like messages in normal and transformed cells. J. Virol.48, 542–546 (1983).
Pinter, A., Lieman-Hurwitz, J., Fleissner, E.: The nature of the association between the murine leukemia virus envelope proteins. Virology91, 345–351 (1978).
Pincus, T.: The endogenous murine type C viruses. In:Stephenson, J. (ed.): Molecular Biology of RNA Tumor Viruses, 77–130. New York: Academic Press 1980.
Rabson, A. B., Steele, P. E., Garon, C. F., Martin, M. A.: mRNA transcripts related to full-length endogenous retroviral DNA in human cells. Nature (London)306, 604–607 (1983).
Rassart, E., Jolicoeur, P.: Restriction analysis and molecular cloning of endogenous murine leukemia virus-specific DNA sequences of the mouse genome. Virology123, 175–186 (1982).
Repaske, R., O'Neill, R. R., Steele, P. E., Martin, M. A.: Characterization and partial nucleotide sequence of endogenous type C retrovirus segments in human chromosomal DNA. Proc. Natl. Acad. Sci. U.S.A.80, 678–682 (1983).
Ruscetti, S., Davis, L., Field, J., Oliff, A.: Friend murine leukemia virus-induced leukemia is associated with the formation of mink cell focus-inducing viruses and is blocked in mice expressing endogenous mink cell focus-inducing xenotropic viral envelope genes. J. Exp. Med.154, 907–920 (1981).
Teich, N.: Taxonomy of retroviruses. In:Weiss, R., Teich, N., Varmus, H., Coffin, J. (eds.). RNA tumor viruses. Molecular Biology of Tumor Viruses, 2nd ed., 25–207. Cold Spring Harbor, N. Y.: Cold Spring Harbor Laboratory publications 1982.
Thomas, P. S.: Hybridization of denatured RNA and small DNA fragments transferred to nitrocellulose. Proc. Natl. Acad. Sci. U.S.A.77, 5201–5205 (1980).
Wejman, J. C., Taylor, B. A., Jenkins, N. A., Copeland, N. G.: Endogenous xenotropic murine leukemia virus-related sequences map to chromosomal regions encoding mouse lymphocyte antigens. J. Virol.50, 237–247 (1984).
Wolff, L., Scolnick, E., Ruscetti, S.: Envelope gene of the Friend spleen focusforming virus: deletion and insertions in 3' gp 70-p 15 E-encoding region have resulted in unique features in the primary structure of its protein product. Proc. Natl. Acad. Sci. U.S.A.80, 4718–4722 (1983).
Wood, T. G., McGeady, M. L., Blair, D. G., Vande Woude, G. F.: Long terminal repeat enhancement of v-mos transforming activity: identification of essential regions. J. Virol.46, 726–736 (1983).
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Robert-Lezenes, J., Moreau-Gachelin, F., Meneceur, P. et al. Retroviral endogenous transcripts related to the envelope gene of friend spleen focus-forming virus in normal mouse tissues. Archives of Virology 90, 15–28 (1986). https://doi.org/10.1007/BF01314141
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DOI: https://doi.org/10.1007/BF01314141