Skip to main content

Evidence for methylation of inactive human rRNA genes in amplified regions

Human Genetics volume 56, pages 315–320 (1981)Cite this article

Summary

In two unrelated families, the short arm of a 14p+ marker chromosome contains an increased number of copies of the 18S+28S rRNA genes without a comparable increase in the transcriptional activity, as shown by silver staining. The DNA in this region is highly enriched in 5-methylcytosine, as shown by specific antibody binding. In contrast, the owl monkey and cat have a single major nucleolus organizer region (NOR) per haploid genome; these NORs contain about the same number of rRNA genes as the 14p+ chromosome but are not methylated. These findings suggest that most of the amplified human rRNA genes on the 14p+ chromosomes have been inactivated by a process involving DNA methylation.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

43,34 €

Price includes VAT (Finland)
Tax calculation will be finalised during checkout.

References

  • De Capoa A, Ferraro M, Menendez F, Mostacci C, Pelliccia F, Rocchi A (1978) Ag-staining of the nucleolus organizer (NO) and its relationship to satellite association. Hum Genet 44: 71–77

    Article  Google Scholar 

  • Court Brown WM, Buckton KE, Jacobs PA, Tough IM, Kuenssberg EV, Knox JDE (1966) Chromosome studies on adults. Cambridge University Press, London

    Google Scholar 

  • Croce CM, Talavera A, Basilico C, Miller OJ (1977) Suppression of the production of mouse 28S ribosomal RNA in mousehuman hybrids segregating mouse chromosomes. Proc Natl Acad Sci USA 74:694–697

    CAS  Article  Google Scholar 

  • Desrosiers RC, Mulder C, Fleckenstein B (1979) Methylation of Herpesvirus saimiri DNA in lymphoid tumor cell lines. Proc Natl Acad Sci USA 76:3839–3843

    CAS  Article  Google Scholar 

  • Doskocil J, Sorm F (1962) Distribution of 5-methylcytosine in pyrimidine sequences of deoxyribonucleic acids. Biochim Biophys Acta 55:953–959

    CAS  Article  Google Scholar 

  • Evans HJ, Buckland RA, Pardue ML (1974) Location of the genes coding for 18S and 28S ribosomal RNA in the human genome. Chromosoma 48:405–426

    CAS  Article  Google Scholar 

  • Flamm WG (1972) Highly repetitive sequences of DNA in chromosomes. Int Rev Cytol 32:1–51

    CAS  Article  Google Scholar 

  • Guntaka RV, Rao PY, Mitsialis SA, Katz R (1980) Modification of avian sarcoma proviral DNA sequences in nonpermissive XC cells but not in permissive chick cells. J Virol 34:569–572

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hamerton JL, Gianelli F, Polani PE (1965) Cytogenetics of Down's syndrome (Mongolism). I. Data on a consecutive series of patients referred for genetic counselling and diagnosis. Cytogenetics 4:171–185

    CAS  Article  Google Scholar 

  • Heitz E (1931) Nukleolen und Chromosomes in der Gattung Vicia. Planta (Berl) 15:495–505

    Article  Google Scholar 

  • Henderson AS, Atwood KC (1976) Satellite-association frequency and rDNA content of a double-satellited chromosome. Hum Genet 31:113–115

    CAS  Article  Google Scholar 

  • Henderson AS, Warburton D, Atwood KC (1972) Location of ribosomal DNA in the human chromosome complement. Proc Natl Acad Sci USA 69:3215–3219

    Article  Google Scholar 

  • Hofgärtner FJ, Schmid M, Krone W, Zenzes MT, Engel W (1979) Pattern of activity of nucleolus organizers during spermatogenesis in mammals as analyzed by silver-staining. Chromosoma 71:197–216

    Article  Google Scholar 

  • Lau YF, Wertelecki W, Pfeiffer RA, Arrighi FE (1979) Cytological analysis of a 14p+ variant by means of N-banding and combinations of silver staining and chromosome bandings. Hum Genet 46:75–82

    CAS  Article  Google Scholar 

  • Lubit BW, Schreck RR, Miller OJ, Erlanger BF (1974) Human chromosome structure as revealed by an immunoperoxidase staining procedure. Exp Cell Res 89:426–429

    CAS  Article  Google Scholar 

  • Lubs HA, Ruddle FH (1970) Application of quantitative karyotyping to chromosome variations. In: Jacobs PA, Price WA, Lane P (eds) Human population cytogenetics. The Williams and Wilkins Co, Baltimore

    Google Scholar 

  • Mandel JL, Chambon P (1979) DNA methylation: organ specific variations in the methylation pattern within and around ovalbumin and other chicken genes. Nucleic Acids Res 7: 2081–2003

    CAS  Article  Google Scholar 

  • McGhee JD, Ginder GD (1979) Specific DNA methylation sites in the vicinity of the chicken β-globin genes. Nature 280: 419–420

    CAS  Article  Google Scholar 

  • Mikelsaar A-VN, Tüür SJ, Käosaar ME (1973) Human karyotype polymorphism. I. Routine and fluorescence microscopic investigation of chromosomes in a normal adult population. Hum Genet 20:89–101

    CAS  Article  Google Scholar 

  • Miller DA, Miller DA, Miller OJ, Tantravahi R, Reese RT (1977) Banded chromosomes of the owl monkey Aotus trivirgatus. Cytogenet Cell Genet 19:215–226

    CAS  Article  Google Scholar 

  • Miller DA, Breg WR, Warburton D, Dev VG, Miller OJ (1978) Regulation of rRNA gene expression in a human 14p+ marker chromosome. Hum Genet 43:289–297

    CAS  Article  Google Scholar 

  • Miller DA, Dev VG, Tantravahi R, Miller OJ (1976) Suppression of human nucleolus organizer activity in mouse-human somatic hybrid cells. Exp Cell Res 101:235–243

    CAS  Article  Google Scholar 

  • Miller OJ, Erlanger BF (1977) Immunological approaches to chromosome banding. In: Human cytogenetics: ICN-UCLA Symposium on Molecular and Cellular Biology, Vol VII. Academic Press, New York, p 87

    Google Scholar 

  • Miller OJ, Miller DA, Dev VG, Tantravahi R, Croce CM (1976) Expression of human and suppression of mouse nucleolus organizer activity in mouse-human somatic cell hybrids. Proc Natl Acad Sci USA 73:4531–4535

    CAS  Article  Google Scholar 

  • Miller OJ, Schnedl W, Allen J, Erlanger BF (1974) 5-Methylcytosine localised in mammalian constitutive heterochromatin. Nature 251:636–637

    CAS  Article  Google Scholar 

  • Miller OJ, Tantravahi R, Miller DA, Yu L-C, Szabo P, Prensky W (1979) Marked increase in ribosomal RNA gene multiplicity in a rat hepatoma cell line. Chromosoma 71:183–195

    CAS  Article  Google Scholar 

  • Petes TD (1980) Unequal meiotic recombination within tandem arrays of yeast ribosomal DNA genes. Cell 19:765–775

    CAS  Article  Google Scholar 

  • Procunier JD, Tartof KD (1978) A genetic locus having trans and contiguous cis functions that control the disproportionate replication of ribosomal RNA genes in Drosophila melanogaster. Genetics 88:67–79

    CAS  PubMed  PubMed Central  Google Scholar 

  • Sahar E, Latt SA (1978) Enhancement of banding patterns in human metaphase chromosomes by energy transfer. Proc Natl Acad Sci USA 75:5650–5604

    CAS  Article  Google Scholar 

  • Sands VE (1969) Short arm enlargement in acrocentric chromosomes. Am J Hum Genet 21:293–304

    CAS  PubMed  PubMed Central  Google Scholar 

  • Schmiady H, Münke M, Sperling K (1979) Ag-staining of nucleolus organizer regions on human prematurely condensed chromosomes from cells with different ribosomal gene activity. Exp Cell Res 121:425–428

    CAS  Article  Google Scholar 

  • Schnedl W (1978) Structure and variability of human chromosomes analyzed by recent techniques. Hum Genet 41:1–9

    CAS  Article  Google Scholar 

  • Schreck RR, Erlanger BF, Miller OJ (1974) The use of antinucleoside antibodies to probe the organization of chromosomes denatured by ultraviolet irradiation. Exp Cell Res 88: 31–39

    CAS  Article  Google Scholar 

  • Spowart G (1978) Triplication of a short arm region of chromosome 15. J Med Genet 15:404–407

    CAS  Article  Google Scholar 

  • Starkman MN, Shaw MW (1967) Atypical acrocentric chromosomes in Negro and Causasian mongols. Am J Hum Genet 19:162–173

    CAS  PubMed  PubMed Central  Google Scholar 

  • Sutter D, Doerfler W (1980) Methylation of integrated adenovirus type 12 DNA sequences in transformed cells is inversely correlated with viral gene expression. Proc Natl Acad Sci USA 77:253–256

    CAS  Article  Google Scholar 

  • Tantravahi U, Guntaka RV, Erlanger BF, Miller OJ (1981) Amplified ribosomal RNA genes in a rat hepatoma cell line are enriched in 5-methylcytosine. Proc Natl Acad Sci USA (in press)

  • Van der Ploeg LHT, Flavell RA (1980) DNA methylation in the human λδβ-globin locus in erythroid and nonerythroid tissues. Cell 19:947–958

    Article  Google Scholar 

  • Warburton D, Atwood KC, Henderson AS (1976) Variation in the number of genes for rRNA among human acrocentric chromosomes: Correlation with frequency of satellite association. Cytogenet Cell Genet 17:221–230

    CAS  Article  Google Scholar 

Download references

Author information

Affiliations

  1. Department of Human Genetics and Development, Columbia University, 10032, New York, NY, USA

    Umadevi Tantravahi & Orlando J. Miller

  2. Department of Microbiology, Columbia University, 10032, New York, NY, USA

    Bernard F. Erlanger

  3. Department of Obstetrics and Gynecology, Columbia University, 10032, New York, NY, USA

    Orlando J. Miller

  4. The Cancer Center/Institute for Cancer Research, College of Physicians and Surgeons, Columbia University, 10032, New York, NY, USA

    Bernard F. Erlanger & Orlando J. Miller

  5. Department of Human Genetics, Yale University, New Haven, USA

    W. Roy Breg

  6. Department of Medical Genetics, University of Southern Alabama, Mobile, USA

    Valdimir Wertelecki

Authors
  1. Umadevi Tantravahi
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. W. Roy Breg
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Valdimir Wertelecki
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Bernard F. Erlanger
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Orlando J. Miller
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Tantravahi, U., Breg, W.R., Wertelecki, V. et al. Evidence for methylation of inactive human rRNA genes in amplified regions. Hum Genet 56, 315–320 (1981). https://doi.org/10.1007/BF00274686

Download citation

  • Received:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00274686

Keywords

  • Methylated
  • Internal Medicine
  • Transcriptional Activity
  • Metabolic Disease
  • Specific Antibody