Skip to main content
Log in

Transcriptional repression mechanisms of nucleolus organizer regions (NORs) in humans and chimpanzees

  • Published:
Chromosome Research Aims and scope Submit manuscript

Abstract

Polymorphisms related to transcriptional inactivation of nucleolus organizer regions (NORs) have long been described in many animals, particularly humans. However, the precise aetiology of such variations is not always clear. We conducted analyses to investigate the repression mechanisms in humans and chimpanzees using FISH (fluorescence in situ hybridisation) with 18 S rDNA, Ag-NOR (silver nitrate) staining, C-banding, and the in situ nick translation technique with the HpaII restriction enzyme. Examination of 48 humans and 46 chimpanzees suggested that there are at least three different mechanisms that produce inactivation of NORs. These include: (1) elimination of rDNA; (2) DNA methylation; (3) gene silencing due to position effects induced by heterochromatin (C-bands) and/or telomeres.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Assum G, Gartmann C, Schempp W, Wöhr G (1994) Evolution of the chAB4 multisequence family in primates. Genomics 21: 34-41.

    Article  PubMed  CAS  Google Scholar 

  • Assum G, Pasantes J, Gläser B, Schempp W, Wöhr G (1998) Concerted evolution of members of the multisequence family chAB4 located on various nonhomologous chromosomes. Mamm Genome 9: 58-63.

    Article  PubMed  CAS  Google Scholar 

  • Bass HW, Marshall WF, Sedat JW, Agard DA, Cande WZ (1997) Telomeres cluster de novo before the initiation of synapsis: a three-dimensional spatial analysis of telomere positions before and during meiotic prophase. J Cell Biol 137: 5-18.

    Article  PubMed  CAS  Google Scholar 

  • de Capoa A, Aleixandre C, Felli MP et al. (1991) Inheritance of ribosomal gene activity and level of DNA methylation in individual gene clusters in a three generation family. Hum Genet 88: 146-152.

    PubMed  CAS  Google Scholar 

  • Ferraro M, Prantera G (1988) Human NORs show correlation between transcriptional activity, DNase I sensitivity, and hypomethylation. Cytogenet Cell Genet 47: 58-61.

    PubMed  CAS  Google Scholar 

  • Ghosh S (1976) The nucleolar structure. Int Rev Cytol 44: 1-28.

    Article  PubMed  CAS  Google Scholar 

  • Goodpasture C, Bloom SE (1975) Visualization of nucleolar organizer regions in mammalian chromosomes using silver staining. Chromosoma 53: 37-50.

    Article  PubMed  CAS  Google Scholar 

  • Greig GM, Willard HF (1992) ?-satellite DNA: characterization and localization of two subfamilies from the distal and proximal short arms of the human acrocentric chromosomes. Genomics 12: 573-580.

    Article  PubMed  CAS  Google Scholar 

  • Henderson AS, Warburton D, Atwood KC (1972) Location of ribosomal DNA in the human chromosome complement. Proc Natl Acad Sci USA 69: 3394-3398.

    Article  PubMed  CAS  Google Scholar 

  • Henderson AS, Atwood KC, Warburton D (1976) Chromosomal distribution of rDNA in Pan paniscus, Gorilla gorilla beringei and Symphalangus syndactylus: comparison to related primates. Chromosoma 59: 147-15.

    Article  PubMed  CAS  Google Scholar 

  • Hirai H (2001) Relationship of telomere sequence and constitutive heterochromatin in the human and apes as detected by PRINS. Meth Cell Sci 23: 29-35.

    Article  CAS  Google Scholar 

  • Hirai H, LoVerde PT (1995) FISH techniques for constructing physical maps on schistosome chromosomes. Parasitol Today 8: 310-314.

    Article  Google Scholar 

  • Hirai H, Hirata M, Aoki Y, Tanaka M, Imai HT (1996) Chiasma analyses of the parasite flukes, Schistosoma and Paragonimus (Trematoda), by using the chiasma distribution graph. Genes Genet Syst 71: 181-188.

    Article  Google Scholar 

  • Hirai H, Hasegawa Y, Kawamoto Y, Tokita E (1998) Tandem duplication of nucleolus organizer region (NOR) in the Japanese macaque Macaca fuscata fuscata. Chromosome Res 6: 191-197.

    Article  PubMed  CAS  Google Scholar 

  • Hirai H, Taguchi T, Godwin AK (1999) Genomic differentiation of 18S ribosomal DNA and ?-satellite DNA in the hominoid and its evolutionary aspects. Chromosome Res 7: 531-540.

    Article  PubMed  CAS  Google Scholar 

  • Hirai H, Hirai Y, Kawamoto Y, Endo H, Kimura J, Rerkamnuaychoke W (2002) Cytogenetic differentiation of two sympatric tree shrew taxa found in the southern part of the Isthmus of Kra. Chromosome Res 10: 313-327.

    Article  PubMed  CAS  Google Scholar 

  • Howell WM, Denton TE, Diamond JR (1975) Differential staining of the satellite regions of human acrocentric chromosomes. Experientia 15: 260-262.

    Article  Google Scholar 

  • Imai HT, Maruyama T, Gojobori T, Inoue Y, Crozier RH (1986) Theoretical bases for karyotype evolution. I. The minimum-interaction hypothesis. Am Nat 128: 900-920.

    Article  Google Scholar 

  • Imai HT, Wada MY, Hirai H, Matsuda Y, Tsuchiya K (1999) Cytological, genetic and evolutionary functions of chiasmata based on chiasma graph analysis. J Theor Biol 198: 239-257.

    Article  PubMed  CAS  Google Scholar 

  • Markovic VD, Worton RG, Berg JM (1978) Evidence for the inheritance of silver-stained nucleolus organizer regions. Hum Gent 41: 181-187.

    CAS  Google Scholar 

  • Meneveri R, Agresti A, Marozzi A et al. (1993) Molecular organization and chromosomal location of human GC-rich heterochromatic blocks. Gene 123: 227-234.

    Article  PubMed  CAS  Google Scholar 

  • Meneveri R, Agresti A, Rocchi M, Marozzi A, Ginelli E (1995) Analysis of GC-rich repetitive nucleotide sequences in great apes. J Mol Evol 40: 405-412.

    Article  PubMed  CAS  Google Scholar 

  • Mikelsaar AV, Schmid M, Krone W, Schwarzacher HG, Schneld W (1977a) Frequency of Ag-stained nucleolus organizer regions in the acrocentric chromosomes of man. Hum Genet 37: 73-77.

    Article  PubMed  CAS  Google Scholar 

  • Mikelsaar AV, Schwarzacher HG, Schnedl W, Wagenbichler P (1977b) Inheritance of Ag-stainability of nucleolus organizer regions: investigation in 7 families with trisomy 21. Hum Genet 38: 183-188.

    Article  PubMed  CAS  Google Scholar 

  • Ofir R, Wong ACC, McDermid HE, Skorecki KL, Selig S (1999) Position effect of human telomeric repeats on replication timing. Proc NatlAcad Sci USA 96: 11434-11439.

    Article  CAS  Google Scholar 

  • O'Neill RJW, O'Neill MJ, Graves JAM (1998) Undermethylation associated with retroelement activation and chromosome remodeling in an interspecific mammalian hybrid. Nature 393: 68-72.

    Article  PubMed  Google Scholar 

  • Roussel P, Hernandez-Verdun D (1994) Identification of Ag-NOR proteins, markers of proliferation related to ribosomal gene activity. Exp Cell Res 214: 465-472.

    Article  PubMed  CAS  Google Scholar 

  • Sumner AT (1972) A simple technique for demonstrating centromeric heterochromatin. Exp Cell Res 75: 304-306.

    Article  PubMed  CAS  Google Scholar 

  • Sumner AT (1990) Chromosome banding. London: Unwin Hyman.

    Google Scholar 

  • Sumner AT (2003) Chromosomes: organization and function. Oxford: Blackwell.

    Google Scholar 

  • Tantravahi R, Miller DA, Dev VG, Miller OJ (1976) Detection of nucleolus organizer regions in chromosomes of human, chimpanzee, gorilla, orangutan and gibbon. Chromosoma 56: 15-27.

    Article  PubMed  CAS  Google Scholar 

  • Tantravahi U, Breg WR, Wertelecki V, Erlanger BF, Miller OJ (1981) Evidence for methylation of inactive human rRNA genes in amplified regions. Hum Genet 56: 315-320.

    Article  PubMed  CAS  Google Scholar 

  • Wada MY, Imai HT (1995) Theoretical analyses of chiasmata using a novel chiasmagraph method applied to Chinese hamsters, mice, and dog. Jpn J Genet 70: 233-265.

    Article  PubMed  CAS  Google Scholar 

  • Wakimoto BT (1998) Beyond the nucleosome: epigenetic aspects of position-effect variegation in Drosophila. Cell 93: 321-324.

    Article  PubMed  CAS  Google Scholar 

  • Wallrath LL (1998) Unfolding the mysteries of heterochromatin. Curr Opin Genet Devel 8: 147-153.

    Article  CAS  Google Scholar 

  • Whitehead CM, Winkfein RJ, Fritzler MJ, Rattner JB (1997) ASE-1: a novel protein of the fibrillar centers of the nucleolus and nucleolus organizer region of mitotic chromosomes. Chromosoma 106: 493-502.

    Article  PubMed  CAS  Google Scholar 

  • Wilson GN (1982) The structure and organization of human ribosomal genes. In: XH. Bush and L. Rothblum, eds. The cell nucleus, Vol. X. New York: Academic Press, pp 287-318.

    Google Scholar 

  • Zakian VA (1995) Saccharomyces telomeres: function, structure, and replication. In: EH. Blackburn and CW. Greider, eds. Telomeres. New York: Cold Spring Harbor Laboratory Press, pp 107-137.

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Hirohisa Hirai.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Guillén, A.K.Z., Hirai, Y., Tanoue, T. et al. Transcriptional repression mechanisms of nucleolus organizer regions (NORs) in humans and chimpanzees. Chromosome Res 12, 225–237 (2004). https://doi.org/10.1023/B:CHRO.0000021911.43225.eb

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/B:CHRO.0000021911.43225.eb

Navigation