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Localizationin situ ofc-myc mRNA andc-myc protein in adult mouse testis

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Summary

It has been suggested that c-myc, one of the proto-oncogenes, plays a role in normal somatic cell proliferation and differentiation. To define whether c-myc is only expressed during somatic cell division or is also expressed during meiotic cell division, the production of c-myc mRNA and protein were investigated in the mouse testis by usingin situ hybridization with non-radioactive DNA probes and enzyme immunohistochemistry respectively. Forin situ hybridization, T-T dimerized DNA probes were used and DNAs hybridizedin situ were detected immunohistochemically using specific antibody against T-T dimer. The results indicate that c-myc mRNA and protein are expressed in a cell-cycle-dependent manner only in spermatogonia and not in spermatocytes and spermatids.

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References

  • Adams, J. C. (1981) Heavy metal intensification of DAB-based HRP reaction product.J. Histochem. Cytochem. 29, 775.

    Google Scholar 

  • Alitalo, K., Ramsay, G., Bishop, J. M., Ohlsson Pfeifer, S., Colby, W. W. &Levinson, A. D. (1983) Identification of nuclear proteins encoded by viral and cellularmyc oncogenes.Nature 306, 274–7.

    Google Scholar 

  • Bellve, A. R., Millette, C. F., Bhatnagar, Y. M. &O'Brien, D. A. (1977) Dissociation of the mouse testis and characterization of isolated spermatogenic cells.J. Histochem. Cytochem. 25, 480–94.

    Google Scholar 

  • Bishop, J. M. (1983) Cellular oncogenes and retroviruses.Annu. Rev. Biochem. 52, 301–54.

    Google Scholar 

  • Blanchard, J.-M., Piechaczyk, M., Dani, C., Chambard, J.-C., Franchi, A., Pouyssegur, J. &Jeanteur, P. (1985) c-myc gene is transcribed at high rate in GO-arrested fibroblasts and is post-transcriptionally regulated in response to growth factors.Nature 317, 443–5.

    Google Scholar 

  • Brahic, M. &Haase, A. T. (1978) Detection of viral sequences of low reiteration frequency byin situ hybridization.Proc. Natl. Acad. Sci. USA 75, 6125–9.

    Google Scholar 

  • Bravo, R., Burckhardt, J., Curran, T. &Muller, R. (1986) Expression of c-fos in NIH3T3 cells is very low but inducible throughout the cell cycle.EMBO J 5, 695–700.

    Google Scholar 

  • Campisi, J., Gray, H. E., Pardee, A. B., Dean, M. &Sonenshein, G. E. (1984). Cell-cycle control of c-myc but not c-ras expression is lost following chemical transformation.Cell. 36, 241–7.

    Google Scholar 

  • Coppola, J. A. &Cole, M. D. (1986) Constitutive c-myc oncogene expression blocks mouse erythroleukaemia cell differentiation but not commitment.Nature 320, 760–3.

    Google Scholar 

  • Dalla-Favera, R., Gelmann, E. P., Martinotti, S., Franchini, G., Papas, T. S., Gallo, R. C. &Wongstall, F. (1982) Cloning and characterization of different human sequences related to the one gene (v-myc) of avian myelocytomatosis virus (MC29).Proc. Natl. Acad. Sci. USA 79, 6497–501.

    Google Scholar 

  • Dani, CH., Blanchard, J. M., Piechaczyk, M., El Sabouty, S., Marty, L. &Jeanteur, PH. (1984) Extreme instability ofmyc mRNA in normal and transformed human cells.Proc. Natl. Acad. Sci. USA 81, 7046–50.

    Google Scholar 

  • Dean, R., Kim, S. S. &Delgado, D. (1986) Expression of c-myc oncogene in human fibroblasts duringin vitro senescence.Biochem. Biophys. Res. Commun. 135, 105–9.

    Google Scholar 

  • Dotto, G. P., Gilman, M. Z., Maruyama, M. &Weinberg, R. A. (1986) c-myc and c-fos expression in differentiating mouse primary keratinocytes.EMBO J. 5, 2853–7.

    Google Scholar 

  • Evan, G. I. &Hancock, D. C. (1985) Studies on the interaction of the human c-myc protein with cell nuclei: p62c-myc as a member of a discrete subset of nuclear proteins.Cell 43, 253–61.

    Google Scholar 

  • Gazin, C., Rigolet, M., Briand, J. P., Van Regenmortel, M. H. V. &Galibert, F. (1986) Immunochemical detection of proteins related to the human c-myc exon 1.EMBO J. 5, 2241–50.

    Google Scholar 

  • Godeau, F., Persson, H., Gray, H. E. &Pardee, A. B. (1986) c-myc expression is dissociated from DNA synthesis and cell division inXenopus oocyte and early embryonic development.EMBO J. 5, 3571–7.

    Google Scholar 

  • Hann, S. R., Thompson, C. B., &Eisenman, R. N. (1985) c-myc oncogene protein synthesis is independent of the cell cycle in human and avian cells.Nature 314, 366–9.

    Google Scholar 

  • Hayashi, S., Gillam, I. G., Delaney, A. D. &Tener, G. M. (1978) Acetylation of chromosome squashes ofDrosophila melanogaster decreases the background in autoradiographs from hybridization with [121I]-labeled RNA.J. Histochem. Cytochem. 26, 677–9.

    Google Scholar 

  • Heikkila, R., Schwab, G., Wickstrom, E., Loke, S. L., Pluznik, D. H., Watt, R. &Neckers, L. M. (1987) A c-myc antisense oligodeoxynucleotide inhibits entry into S phase but not progress from G0 to G1.Nature 328, 445–9.

    Google Scholar 

  • Izumi, S., Sekino, M., Moriuchi, T., Koji, T., Takasaki, Y., Yanaihara, C., Yanaihara, N., Abe, K. &Nakane, P. K. (1987) Mode of PCNA/cyclin and c-myc antigens in regenerating rat livers.Acta Histochem. Cytochem. 20, 710.

    Google Scholar 

  • Izumi, S., Moriuchi, T., Koji, T., Tanno, M., Terashima, K., Iguchi, K., Mochizuki, T., Yanaihara, C., Yanaihara, N., Abe, K. & Nakane, P. K. (1988) Localization of c-myc in HL-60 cells, neoplastic and normal tissues: an immunohistochemical andin situ hybridization study.Acta Histochem, Cytochem,21, in press.

  • Kelly, K., Cochran, B. H., Stiles, C. D. &Leder, P. (1983) Cell-specific regulation of the c-myc gene by lymphocyte mitogens and platelet-derived growth factor.Cell 35, 603–10.

    Google Scholar 

  • Kruijer, W., Skelly, H., Botteri, F., Van Der Putten, Barber, J. R., Verma, I. M. &Leffert, H. L. (1986) Proto-oncogene expression in regenerating liver is simulated in cultures of primary adult rat hepatocytes.J. Biol. Chem. 261, 7929–33.

    Google Scholar 

  • Lachman, H. M. &Skoultchi, A. I. (1984) Expression of c-myc changes during differentiation of mouse erythroleukaemia cells.Nature 310, 592–4.

    Google Scholar 

  • Levine, L., Seaman, E., Hammerschlag, E. &Van Vunakis, H. (1966) Antibodies to photoproducts of deoxyribonucleic acids irradiated with ultraviolet light.Science 153, 1666–7.

    Google Scholar 

  • Makino, R., Hayashi, K. &Sugimura, T. (1984) c-myc transcript is induced in rat liver at a very early stage of regeneration or by cycloheximide treatment.Nature 310, 697–8.

    Google Scholar 

  • Monesi, V. (1964) Ribonucleic acid synthesis during mitosis and meiosis in the mouse testis.J. Cell Biol 22, 521–32.

    Google Scholar 

  • Nakane, P. K., Moriuchi, T., Koji, T., Tanno, M. &Abe, K. (1987)In situ localization of mRNA using thyminethymine dimerized cDNA.Acta Histochem. Cytochem. 20, 229–43.

    Google Scholar 

  • Nakane P. K. &Pierce, G. B. (1966) Enzyme-labeled antibodies: Preparation and application for localization of antigens.J. Histochem. Cytochem. 14, 929–31.

    Google Scholar 

  • Nath, P., Getzenberg, R., Beebe, D., Pallansch, L. &Zelenka, P. (1987) c-myc mRNA is elevated as differentiating lens cells withdraw from the cell cycle.Exp. Cell Res. 169, 215–22.

    Google Scholar 

  • Oakberg, E. F. (1971) Spermatogonial stem-cell renewal in the mouse.Anat. Rec. 169, 515–32.

    Google Scholar 

  • Ono, T., Tawa, R., Shinya, K., Hirose, S. &Okada, S. (1986) Methylation of the c-myc gene changes during aging process of mice.Biochem. Biophys. Res. Commun. 139, 1299–304.

    Google Scholar 

  • Persson, H., Hennighausen, L., Traub, R. Degrado, W. &Leder, P. (1984) Antibodies to human c-myc oncogene product: Evidence of an evolutionarily conserved protein induced during cell proliferation.Science 225, 687–93.

    Google Scholar 

  • Persson, H. &Leder, P. (1984) Nuclear localization and DNA binding properties of a protein expressed by human c-myc oncogene.Science 225, 718–20.

    Google Scholar 

  • Pfeifer-Ohlsson, S., Goustin, A. S., Rydnert, J., Wahlstrom, T., Bjersing, L., Stehelin, D. &Ohlsson, R. (1984) Spatial and temporal pattern of cellularmyc oncogene expression in developing human placenta: Implications for embryonic cell proliferation.Cell 38, 585–96.

    Google Scholar 

  • Pfeifer-Ohlsson, S., Rydnert, J., Goustin, A. S., Larsson, E., Betsholtz, C. &Ohlsson, R. (1985) Cell-type-specific pattern ofmyc protooncogene expression in developing human embryos.Proc. Natl. Acad. Sci. USA 82, 5050–4.

    Google Scholar 

  • Rabbitts, P. H., Watson, J. V., Lamond, A., Forster, A., Stinson, M. A., Evan, G., Fischer, W., Atherton, E., Sheppard, R. &Rabbitts, T. H. (1985) Metabolism of c-myc gene products: c-myc mRNA and protein expression in the cell cycle.EMBO J. 4, 2009–15.

    Google Scholar 

  • Ramsay, G., Evan, G. I. & Bishop, M. (1984) The protein encoded by the human proto-oncogene c-myc.Proc. Natl. Acad. Sci. USA. 81, 7742–6.

    Google Scholar 

  • Sejersen, T., Sumegi, J. &Ringertz, N. R. (1985) Density-dependent arrest of DNA replication is accompanied by decreased levels of c-myc mRNA in myogenic but not differentiation-defective myoblasts.J. Cell. Physiol. 125, 465–70.

    Google Scholar 

  • Stewart, T. A., Bellve, A. R. &Leder, P. (1984) Transcription and promoter usage of themyc gene in normal somatic and spermatogenic cells.Science 226, 707–10.

    Google Scholar 

  • Studzinski, G. P., Brelvi, Z. S., Feldman, S. C. &Watt, R. A. (1986) Participation of c-myc protein in DNA synthesis of human cells.Science 234, 467–70.

    Google Scholar 

  • Taylor, M. V., Gusse, M., Evan, G. I., Dathan, N. &Mechali, M. (1986)Xenopus myc proto-oncogene during development: Expression as a stable maternal mRNA uncoupled from cell division.EMBO J. 5, 3563–70.

    Google Scholar 

  • Thompson, C. B., Challoner, P. B., Neiman, P. E. &Groudine, M. (1985) Levels of c-myc oncogene mRNA are invariant throughout the cell cycle.Nature 314, 363–6.

    Google Scholar 

  • Watanabe, T., Sariban, E., Mitchell, T. &Kufe, D. (1985) Human c-myc and N-ras expression during induction of HL-60 cellular differentiation.Biochem. Biophys. Res. Commun. 126, 999–1005.

    Google Scholar 

  • Westin, E. H., Wong-Staal, F., Gelmann, E. P., Dalla Favera, R., Papas, T. S., Lautenberger, J. A., Eva, A., Reddy, E. P., Tronick, S. R., Aaronson, S. A. &Gallo, R. C. (1982) Expression of cellular homologues of retroviralonc genes in human hematopoietic cells.Proc. Natl. Acad. Sci. USA 79, 2490–4.

    Google Scholar 

  • Wilson, M. B. &Nakane, P. K. (1978) Recent developments in the periodate method of conjugating horseradish peroxidase (HRPO) to antibodies. InImmunofluorescence and Related Staining Techniques (edited byKnapp, W., Holubar, K. &Wick, G.), pp. 215–24. Amsterdam: Elsevier/North-Holland Biomedical Press.

    Google Scholar 

  • Winqvist, R., Saksela, K. &Alitalo, K. (1984) Themyc proteins are not associated with chromatin in mitotic cells.EMBO J. 3, 2947–50.

    Google Scholar 

  • Yen, A. &Guernsey, D. L. (1986) Increased c-myc RNA levels associated with the precommitment state during HL-60 myeloid differentiation.Cancer Res. 46, 4156–61.

    Google Scholar 

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Authors and Affiliations

  1. Department of Cell Biology, Tokai University School of Medicine, Bohseidai, 259-11, Isehara, Japan

    Takehiko Koji, Shinichi Izumi, Masashi Tanno, Tetsuya Moriuchi & Paul K. Nakane

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  1. Takehiko Koji
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  2. Shinichi Izumi
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  3. Masashi Tanno
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  4. Tetsuya Moriuchi
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  5. Paul K. Nakane
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Koji, T., Izumi, S., Tanno, M. et al. Localizationin situ ofc-myc mRNA andc-myc protein in adult mouse testis. Histochem J 20, 551–557 (1988). https://doi.org/10.1007/BF01002609

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  • DOI: https://doi.org/10.1007/BF01002609

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