Advertisement

Mammalian Genome

, Volume 6, Issue 2, pp 76–83 | Cite as

Transcripts from opposite strands of γ satellite DNA are differentially expressed during mouse development

  • F. Rudert
  • S. Bronner
  • J. -W. Garnier
  • P. Dollé
Original Contributions

Abstract

Using in vitro immuno-selected retinoic acid response elements, we have isolated mouse genomic clones containing major (γ) satellite DNA repeats that are considered as typical of chromosome centromeres. Several cDNA clones were then isolated from a F9 cell cDNA library and were found to harbor variants of the 234-base pair consensus γ satellite monomer. In Northern analysis, these satellite DNA sequences hybridized predominantly to an ≈1.8-kb RNA species in polyadenylated RNA from P19 cells. These transcripts were strongly repressed by retinoic acid, and nuclear run-on assays revealed that this repression was, at least in part, mediated at the transcriptional level. Satellite transcripts were also detected in HeLa cells, where they were similarly down-regulated by retinoids. Heterogeneously sized satellite transcripts were detected in RNA from specific mouse tissues, such as fetuses (but not placenta), adult liver, and testis. In situ hybridization analysis revealed that satellite transcripts are generated from opposite DNA strands and are differentially expressed in cells of the developing central nervous system as well as in adult liver and testis. These data may have implications on retinoic acid-mediated transcriptional regulation and centromere function.

Keywords

Retinoic Acid Retinoid Adult Liver Centromere Function Retinoic Acid Response Element 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Auffray, C., Rougeon, F. (1980). Purification of mouse immunoglobulin heavy-chain messenger RNAs from total myeloma tumor RNA. Eur. J. Biochem. 107, 303–314.Google Scholar
  2. Buttner, K.A., Lo, C.W. (1986). High frequency DNA rearrangements associated with mouse centromeric satellite DNA. J. Mol. Biol. 187, 547–556.Google Scholar
  3. Chomezynski, P., Sacchi, N. (1987). Single-step method of RNA isolation by guanidinium thiocyanate-phenol-chloroform extraction. Anal. Biochem. 162, 156–159.Google Scholar
  4. Choo, K.H., Brown, R., Webb, G., Craig, I.W., Filby, R.G. (1987). Genomic organization of human centromeric alpha satellite DNA: Characterization of a chromosome 17 alpha satelite sequence. DNA 6, 297–305.Google Scholar
  5. Décimo, D., Georges-Labouesse, E., Dollé, P. (1994). In situ hybridization of nucleic acid probes to cellular RNA. In Gene Probes: A Practical Approach, Vol. II, B.D. Hames, S.J. Higgins, eds. (Oxford, UK: Oxford University Press), in press.Google Scholar
  6. De Luca, L.M. (1991). Retinoids and their receptors in differentiation, embryogenesis, and neoplasia. FASEB J. 5, 2924–2932.Google Scholar
  7. deThé, H., Vivanco-Ruiz, M.d.M., Tiollais, P., Stunnenberg, H., Dejean, A. (1990). Identification of a retinoic acid responsive element in the retinoic acid receptor β gene. Nature 343, 77–180.Google Scholar
  8. Diaz, M.O., Barsacchi-Pilone, G., Mahon, K.A., Gall, J.G. (1981). Transcripts from both strands of satellite DNA occur on lampbrush chromosome loops of the newt Notophthalamus. Cell 24, 649–659.Google Scholar
  9. Draetta, G. (1990). Cell cycle control in eukaryotes: molecular mechanisms of cdc2 activation. Trends Biochem. Sci. 15, 378–383.Google Scholar
  10. Durand, B., Saunders, M., Leroy, P., Rees, J., Chambon, P. (1992). Alltrans and 9-cis retinoic acid induction of CRABPII transcription is mediated by RAR-RXR heterodimers bound to DR1 and DR2 repeated motifs. Cell 71, 73–85.Google Scholar
  11. Feinberg, A.P., Vogelstein, B. (1983). A technique for radiolabeling restriction endonuclease fragments to high specific activity. Anal. Biochem. 132, 6–13.Google Scholar
  12. Gaubatz, J.W., Cutler, R.G. (1990). Mouse satellite DNA is transcribed in senescent cardiac muscle. J. Biol. Chem. 265, 17753–17758.Google Scholar
  13. Grosveld, F.G., Lund, T., Murray, E.J., Mellor, A.L., Dahl, H.H.M., Flavell, R.A. (1982). The construction of cosmid libraries which can be used to transform eukaryotic cells. Nucleic Acids Res. 10, 6715–6732.Google Scholar
  14. Haigwood, N.L., Jahn, C.L., Hutchinson, A., Edgell, M.H. (1981). Location in three repetitive sequence families found in BALB/c adult β globin genes. Nucleic Acids Res. 9, 133–1150.Google Scholar
  15. Horz, W., Altenburger, W. (1981). Nucleotide sequence of mouse satellite DNA. Nucleic Acids Res. 9, 683–696.Google Scholar
  16. Howell, J.M., Thompson, J.N., Pitt, G.A.J. (1963). Histology of the lesions produced in the reproductive tract of animals fed a diet deficient of vitamin A acid. I. The male rat. J. Reprod. Fertil. 5, 159–167.Google Scholar
  17. Jackson, M.S., Mole, S.E., Ponder, B.A.J. (1992). Characterization of a boundary between satellite III and alphoid sequences on human chromosome 10. Nucleic Acids Res. 20, 4781–4787.Google Scholar
  18. Jagadeeswaran, P., Forget, B.G., Weissman, S.M. (1981). Short interspersed repetitive DNA elements in eucaryotes: transposable DNA elements generated by reverse trancription of RNA pol III transcripts? Cell 26, 141–142.Google Scholar
  19. Johnson, D.J., Kroisel, P.M., Klapper, H.J., Rosenkranz, W. (1992). Microdissection of a human marker chromosome reveals its origin and a new family of centromeric repetitive DNA. Hum. Mol. Genet. 1, 741–747.Google Scholar
  20. Krayev, A.S., Kramerov, D.A., Skryabin, K.G., Ryskov, A.P., Bayev, A.A., Georgiev, G.P. (1980). The nucleotide sequence of the ubiquitous repetitive DNA sequence B1 complementary to the most abundant class of mouse fold-back RNA. Nucleic Acids Res. 8, 1201–1215.Google Scholar
  21. Leid, M., Kastner, P., Chambon, P. (1992). Multiplicity generates diversity in the retinoic acid signalling pathways. Trends Biochem. Sci. 17, 427–433.Google Scholar
  22. Linial, M., Gunderson, N., Groudine, M. (1985). Enhanced transcription of c-myc in bursal lymphoma cells requires continuous protein synthesis. Science 230, 1126–1132.Google Scholar
  23. Lipkin, S.M., Nelson, C.A., Glass, C.K., Rosenfeld, M.G. (1992). A negative retinoic acid response element in the rat oxytocin promoter restricts transcriptional stimulation by heterologous transactivation domains. Proc. Natl. Acad. Sci. USA 89, 1209–1213.Google Scholar
  24. Lufkin, T., Lohnes, D., Mark, M., Dierich, A., Gorry, P., Gaub, M.-P., LeMeur, M., Chambon, P. (1993). High postnatal lethality and testis degeneration in retinoic acid receptor α mutant mice. Proc. Natl. Acad. Sci. USA 90, 7225–7229.Google Scholar
  25. Maraia, R.J. (1991). The subset of mouse B1 (Alu-equivalent) sequences expressed as small processed cytoplasmic transcripts. Nucleic Acids Res. 19, 5695–5702.Google Scholar
  26. Nagpal, S., Saunders, M., Kastner, P., Durand, B., Nakshatri, H., Chambon, P. (1992). Promoter context- and response element-dependent specificity of the transcriptional activation and modulating functions of retinoic acid receptors. Cell 70, 1007–1019.Google Scholar
  27. Oakberg, J. (1956). Duration of spermatogenesis in the mouse and timing of stages of the cycle of the seminiferous epithelium. Am. J. Anat. 99, 504–516.Google Scholar
  28. Potter, S.S., Jones, R.S. (1983). Unusual junctions of human alphoid satellite DNA with contiguous non-satellite sequences: sequence analysis of junction regions. Nucleic Acids Res. 11, 3137–3153.Google Scholar
  29. Ragsdale, C.W. Jr., Brockes, J.P. (1991). Retinoids and their targets in vertebrate development. Curr. Opin. Cell Biol. 3, 928–934.Google Scholar
  30. Rudert, F., Gronemeyer, H. (1993). Retinoic acid-response elements with a highly repetitive structure isolated by immuno-selection from genomic DNA. J. Steroid Biochem. Mol. Biol. 46, 121–133.Google Scholar
  31. Rudert, F., Garnier, J.-M., Schuhbaur, B. (1993). Cloning of a pseudogene and cDNA encoding a 17-kDa ribosomal protein from mouse: structure and regulation of expression. Gene 133, 249–254.Google Scholar
  32. Schrewe, H., Thompson, J., Bona, M., Hefta, L.J.F., Maruya, A., Hassauer, M., Shively, J.E., von Kleist, S., Zimmermann, W. (1990). Cloning of the complete gene for the carcinoembryonic antigen: analysis of its promoter indicates a region conveying cell type-specific expression. Mol. Cell. Biol. 10, 2738–2748.Google Scholar
  33. Sleigh, M.J. (1992). Differentiation and proliferation in mouse embryonal carcinoma cells. BioEssays 14, 769–775.Google Scholar
  34. Smith, G.P. (1976). Evolution of repeated DNA sequences by unequal crossover. Science 191, 528–535.Google Scholar
  35. Stephenson, E.C., Erba, H.P., Gall, J.G. (1981). Histone gene clusters of the newt Notophthalamus are separated by long tracts of satellite DNA. Cell 24, 639–647.Google Scholar
  36. Van Arsdell, S.W., Denison, R.A., Bernstein, L.B., Weiner, A.M. (1981). Direct repeats flank three small nuclear RNA pseudogenes in the human genome. Cell 26, 11–17.Google Scholar
  37. Van Pelt, H.M.M., De Rooij, D.G. (1991). Retinoic acid is able to reinitiate spermatogenesis in vitamin A-deficient rats and high replicate doses support the full development of spermatogenic cells. Endocrinology 128, 697–704.Google Scholar
  38. Vasios, G.W., Gold, J.D., Petkovich, M., Chambon, P., Gudas, L.J. (1989). A retinoic acid-responsive element is present in the 5′ flanking region of the laminin B1 gene. Proc. Natl. Acad. Sci. USA 86, 9099–9103.Google Scholar
  39. Vissel, B., Choo, K.H. (1989). Mouse major (γ) satellite DNA is highly conserved and organized into extremely long tanden arrays: implications for recombination between nonhomologous chromosomes. Genomics 5, 407–414.Google Scholar
  40. Wevrick, R., Willard, V.P., Willard, H.F. (1992). Structure of DNA near long tandem arrays of alpha satellite DNA at the centromere of human chromosome 7. Genomics 14, 912–923.Google Scholar
  41. Willard, H.F. (1990). Centromeres of mammalian chromosomes. Trends Genet. 6, 410–416.Google Scholar
  42. Wong, A.K.C., Rattner, A.B. (1988). Sequence organization and cytological localization of the minor satellite of mouse. Nucleic Acids Res. 16, 11645–11661.Google Scholar
  43. Zelent, A., Mendelsohn, C., Kastner, P., Krust, A., Garnier, J.-M., Ruffenach, F., Leroy, P., Chambon, P. (1991). Differentially expressed isoforms of the mouse retinoic acid receptor β are generated by usage of two promoters and alternative splicing. EMBO J. 10, 71–81.Google Scholar
  44. Zimmermann, W., Ortlieb, B., Friedrich, R., von Kleist, S. (1987). Isolation and characterization of cDNA clones encoding the human carcinoembryonic antigen reveal a highly conserved repeating structure. Proc. Natl. Acad. Sci. USA 84, 2960–2964.Google Scholar

Copyright information

© Springer-Verlag New York Inc. 1995

Authors and Affiliations

  • F. Rudert
    • 1
  • S. Bronner
    • 1
  • J. -W. Garnier
    • 1
  • P. Dollé
    • 1
  1. 1.Laboratoire de Génétique Moléculaire des Eucaryotes du CNRS, Unité 184 de Biologie Moléculaire et de Génie, Génétique de l'INSERMIGBMCILLKIRCH CedexFrance

Personalised recommendations