Skip to main content
NCBI home page
Nucleic Acids Research logoLink to Nucleic Acids Research
. 1997 Dec 1;25(23):4740–4747. doi: 10.1093/nar/25.23.4740

Human genes encoding U3 snRNA associate with coiled bodies in interphase cells and are clustered on chromosome 17p11.2 in a complex inverted repeat structure.

L Gao 1, M R Frey 1, A G Matera 1
PMCID: PMC147103  PMID: 9365252

Abstract

Coiled bodies (CBs) are nuclear organelles whose morphological structure and molecular composition have been conserved from plants to animals. Furthermore, CBs are often found to co-localize with specific DNA loci in both mammalian somatic nuclei and amphibian oocytes. Much as rDNA sequences are called nucleolus organizers, we term these coiled body-associated sequences 'coiled body organizers' (CBORs). The only sequences that have been shown to be CBORs in human cells are the U1, U2 and histone gene loci. We wanted to determine whether other snRNA genes might also act as CBORs. In this paper we show that human U3 genes (the RNU3 locus) preferentially associate with CBs in interphase cells. In addition, we have analyzed the genomic organization of the RNU3 locus by constructing a BAC and P1 clone contig. We found that, unlike the RNU1 and RNU2 loci, U3 genes are not tandemly repeated. Rather, U3 genes are clustered on human chromosome 17p11.2, with evidence for large inverted duplications within the cluster. Thus all of the CBORs identified to date are composed of either tandemly repeated or tightly clustered genes. The evolutionary and cell biological consequences of this type of organization are discussed.

Full Text

The Full Text of this article is available as a PDF (309.0 KB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Bauer D. W., Murphy C., Wu Z., Wu C. H., Gall J. G. In vitro assembly of coiled bodies in Xenopus egg extract. Mol Biol Cell. 1994 Jun;5(6):633–644. doi: 10.1091/mbc.5.6.633. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Beven A. F., Simpson G. G., Brown J. W., Shaw P. J. The organization of spliceosomal components in the nuclei of higher plants. J Cell Sci. 1995 Feb;108(Pt 2):509–518. doi: 10.1242/jcs.108.2.509. [DOI] [PubMed] [Google Scholar]
  3. Callan H. G., Gall J. G., Murphy C. Histone genes are located at the sphere loci of Xenopus lampbrush chromosomes. Chromosoma. 1991 Dec;101(4):245–251. doi: 10.1007/BF00365156. [DOI] [PubMed] [Google Scholar]
  4. Chan E. K., Takano S., Andrade L. E., Hamel J. C., Matera A. G. Structure, expression and chromosomal localization of human p80-coilin gene. Nucleic Acids Res. 1994 Oct 25;22(21):4462–4469. doi: 10.1093/nar/22.21.4462. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Chevillard C., Le Paslier D., Passage E., Ougen P., Billault A., Boyer S., Mazan S., Bachellerie J. P., Vignal A., Cohen D. Relationship between Charcot-Marie-Tooth 1A and Smith-Magenis regions. snU3 may be a candidate gene for the Smith-Magenis syndrome. Hum Mol Genet. 1993 Aug;2(8):1235–1243. doi: 10.1093/hmg/2.8.1235. [DOI] [PubMed] [Google Scholar]
  6. Frey M. R., Matera A. G. Coiled bodies contain U7 small nuclear RNA and associate with specific DNA sequences in interphase human cells. Proc Natl Acad Sci U S A. 1995 Jun 20;92(13):5915–5919. doi: 10.1073/pnas.92.13.5915. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Gall J. G., Stephenson E. C., Erba H. P., Diaz M. O., Barsacchi-Pilone G. Histone genes are located at the sphere loci of newt lampbrush chromosomes. Chromosoma. 1981;84(2):159–171. doi: 10.1007/BF00399128. [DOI] [PubMed] [Google Scholar]
  8. Gall J. G., Tsvetkov A., Wu Z., Murphy C. Is the sphere organelle/coiled body a universal nuclear component? Dev Genet. 1995;16(1):25–35. doi: 10.1002/dvg.1020160107. [DOI] [PubMed] [Google Scholar]
  9. Görlich D., Mattaj I. W. Nucleocytoplasmic transport. Science. 1996 Mar 15;271(5255):1513–1518. doi: 10.1126/science.271.5255.1513. [DOI] [PubMed] [Google Scholar]
  10. Henry R. W., Sadowski C. L., Kobayashi R., Hernandez N. A TBP-TAF complex required for transcription of human snRNA genes by RNA polymerase II and III. Nature. 1995 Apr 13;374(6523):653–656. doi: 10.1038/374653a0. [DOI] [PubMed] [Google Scholar]
  11. Hughes J. M., Ares M., Jr Depletion of U3 small nucleolar RNA inhibits cleavage in the 5' external transcribed spacer of yeast pre-ribosomal RNA and impairs formation of 18S ribosomal RNA. EMBO J. 1991 Dec;10(13):4231–4239. doi: 10.1002/j.1460-2075.1991.tb05001.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Jeffreys A. J., Tamaki K., MacLeod A., Monckton D. G., Neil D. L., Armour J. A. Complex gene conversion events in germline mutation at human minisatellites. Nat Genet. 1994 Feb;6(2):136–145. doi: 10.1038/ng0294-136. [DOI] [PubMed] [Google Scholar]
  13. Jiménez-García L. F., Segura-Valdez M. L., Ochs R. L., Rothblum L. I., Hannan R., Spector D. L. Nucleologenesis: U3 snRNA-containing prenucleolar bodies move to sites of active pre-rRNA transcription after mitosis. Mol Biol Cell. 1994 Sep;5(9):955–966. doi: 10.1091/mbc.5.9.955. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Juyal R. C., Figuera L. E., Hauge X., Elsea S. H., Lupski J. R., Greenberg F., Baldini A., Patel P. I. Molecular analyses of 17p11.2 deletions in 62 Smith-Magenis syndrome patients. Am J Hum Genet. 1996 May;58(5):998–1007. [PMC free article] [PubMed] [Google Scholar]
  15. Karpen G. H., Schaefer J. E., Laird C. D. A Drosophila rRNA gene located in euchromatin is active in transcription and nucleolus formation. Genes Dev. 1988 Dec;2(12B):1745–1763. doi: 10.1101/gad.2.12b.1745. [DOI] [PubMed] [Google Scholar]
  16. Kass S., Tyc K., Steitz J. A., Sollner-Webb B. The U3 small nucleolar ribonucleoprotein functions in the first step of preribosomal RNA processing. Cell. 1990 Mar 23;60(6):897–908. doi: 10.1016/0092-8674(90)90338-f. [DOI] [PubMed] [Google Scholar]
  17. Lamond A. I., Carmo-Fonseca M. The coiled body. Trends Cell Biol. 1993 Jun;3(6):198–204. doi: 10.1016/0962-8924(93)90214-l. [DOI] [PubMed] [Google Scholar]
  18. Liao D., Pavelitz T., Kidd J. R., Kidd K. K., Weiner A. M. Concerted evolution of the tandemly repeated genes encoding human U2 snRNA (the RNU2 locus) involves rapid intrachromosomal homogenization and rare interchromosomal gene conversion. EMBO J. 1997 Feb 3;16(3):588–598. doi: 10.1093/emboj/16.3.588. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Lichter P., Tang C. J., Call K., Hermanson G., Evans G. A., Housman D., Ward D. C. High-resolution mapping of human chromosome 11 by in situ hybridization with cosmid clones. Science. 1990 Jan 5;247(4938):64–69. doi: 10.1126/science.2294592. [DOI] [PubMed] [Google Scholar]
  20. Matera A. G., Tycowski K. T., Steitz J. A., Ward D. C. Organization of small nucleolar ribonucleoproteins (snoRNPs) by fluorescence in situ hybridization and immunocytochemistry. Mol Biol Cell. 1994 Dec;5(12):1289–1299. doi: 10.1091/mbc.5.12.1289. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Matera A. G., Weiner A. M., Schmid C. W. Structure and evolution of the U2 small nuclear RNA multigene family in primates: gene amplification under natural selection? Mol Cell Biol. 1990 Nov;10(11):5876–5882. doi: 10.1128/mcb.10.11.5876. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Mazan S., Bachellerie J. P. Organization of the gene family encoding mouse U3B RNA: role of gene conversions in its concerted evolution. Gene. 1990 Oct 15;94(2):263–272. doi: 10.1016/0378-1119(90)90397-a. [DOI] [PubMed] [Google Scholar]
  23. Mazan S., Mattéi M. G., Roeckel N., Qu L. H., Bachellerie J. P. In humans all U3 genes map to chromosome 17p12-->p11, but in mouse the U3A and U3B genes are located on different chromosomes. Cytogenet Cell Genet. 1993;62(4):203–206. doi: 10.1159/000133476. [DOI] [PubMed] [Google Scholar]
  24. Pavelitz T., Rusché L., Matera A. G., Scharf J. M., Weiner A. M. Concerted evolution of the tandem array encoding primate U2 snRNA occurs in situ, without changing the cytological context of the RNU2 locus. EMBO J. 1995 Jan 3;14(1):169–177. doi: 10.1002/j.1460-2075.1995.tb06987.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Roth M. B. Spheres, coiled bodies and nuclear bodies. Curr Opin Cell Biol. 1995 Jun;7(3):325–328. doi: 10.1016/0955-0674(95)80086-7. [DOI] [PubMed] [Google Scholar]
  26. Sadowski C. L., Henry R. W., Kobayashi R., Hernandez N. The SNAP45 subunit of the small nuclear RNA (snRNA) activating protein complex is required for RNA polymerase II and III snRNA gene transcription and interacts with the TATA box binding protein. Proc Natl Acad Sci U S A. 1996 Apr 30;93(9):4289–4293. doi: 10.1073/pnas.93.9.4289. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Savino R., Gerbi S. A. In vivo disruption of Xenopus U3 snRNA affects ribosomal RNA processing. EMBO J. 1990 Jul;9(7):2299–2308. doi: 10.1002/j.1460-2075.1990.tb07401.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Smith C. M., Steitz J. A. Sno storm in the nucleolus: new roles for myriad small RNPs. Cell. 1997 May 30;89(5):669–672. doi: 10.1016/s0092-8674(00)80247-0. [DOI] [PubMed] [Google Scholar]
  29. Smith K. P., Carter K. C., Johnson C. V., Lawrence J. B. U2 and U1 snRNA gene loci associate with coiled bodies. J Cell Biochem. 1995 Dec;59(4):473–485. doi: 10.1002/jcb.240590408. [DOI] [PubMed] [Google Scholar]
  30. Suh D., Wright D., Reddy R. Sequences more than 500 base pairs upstream of the human U3 small nuclear RNA gene stimulate the synthesis of U3 RNA in frog oocytes. Biochemistry. 1991 Jun 4;30(22):5438–5443. doi: 10.1021/bi00236a016. [DOI] [PubMed] [Google Scholar]
  31. Tuma R. S., Stolk J. A., Roth M. B. Identification and characterization of a sphere organelle protein. J Cell Biol. 1993 Aug;122(4):767–773. doi: 10.1083/jcb.122.4.767. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Wu C. H., Murphy C., Gall J. G. The Sm binding site targets U7 snRNA to coiled bodies (spheres) of amphibian oocytes. RNA. 1996 Aug;2(8):811–823. [PMC free article] [PubMed] [Google Scholar]
  33. Wu Z., Murphy C., Gall J. G. Human p80-coilin is targeted to sphere organelles in the amphibian germinal vesicle. Mol Biol Cell. 1994 Oct;5(10):1119–1127. doi: 10.1091/mbc.5.10.1119. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Yoon J. B., Roeder R. G. Cloning of two proximal sequence element-binding transcription factor subunits (gamma and delta) that are required for transcription of small nuclear RNA genes by RNA polymerases II and III and interact with the TATA-binding protein. Mol Cell Biol. 1996 Jan;16(1):1–9. doi: 10.1128/mcb.16.1.1. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Yuan Y., Reddy R. Genes for human U3 small nucleolar RNA contain highly conserved flanking sequences. Biochim Biophys Acta. 1989 Jun 1;1008(1):14–22. doi: 10.1016/0167-4781(89)90164-4. [DOI] [PubMed] [Google Scholar]

Articles from Nucleic Acids Research are provided here courtesy of Oxford University Press

RESOURCES