Transcription-dependent Colocalization of the U1, U2, U4/U6, and U5 SnRNPs in Coiled Bodies

Overview

Journal J Cell Biol

Specialty Cell Biology

Date 1992 Apr 1

PMID 1532583

Citations 176

Authors

M Carmo-Fonseca

R Pepperkok

M T Carvalho

A I Lamond

Affiliations

Soon will be listed here.

Abstract

We have recently shown that discrete foci are present in the nuclei of mammalian cells in which each of the U1, U2, U4/U6, and U5 snRNPs involved in pre-mRNA splicing, and the non-snRNP-splicing factor U2AF, are concentrated (Carmo-Fonseca, M., D. Tollervey, R. Pepperkok, S. Barabino, A. Merdes, C. Brunner, P. D. Zamore, M. R. Green, E. Hurt, and A. I. Lamond. 1991. EMBO (Eur. Mol. Biol. Organ.) J. 10:195-206; Carmo-Fonseca, M., R. Pepperkok, B. S. Sproat, W. Ansorge, M. S. Swanson, and A. I. Lamond. 1991 EMBO (Eur. Mol. Biol. Organ.) J. 10:1863-1873). Here, we identify these snRNP-rich organelles as coiled bodies. snRNPs no longer concentrate in coiled bodies after cells are treated with the transcription inhibitors alpha-amanitin or actinomycin D. snRNP association with coiled bodies is also disrupted by heat shock. This indicates that the association of snRNPs with coiled bodies may be connected with the metabolism of nascent transcripts. A novel labeling method is described which shows both the RNA and protein components of individual snRNPs colocalizing in situ. Using this procedure all spliceosomal snRNPs are seen distributed in a nonhomogeneous pattern throughout the nucleoplasm, excluding nucleoli. They are most concentrated in coiled bodies, but in addition are present in "speckled" structures which are distinct from coiled bodies and which contain the non-snRNP splicing factor SC-35. U1 snRNP shows a more widespread nucleoplasmic staining, outside of coiled bodies and "speckled" structures, relative to the other snRNPs. The association of snRNPs with "speckles" is disrupted by heat shock but enhanced when cells are treated with alpha-amanitin.

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References

Bond U . Heat shock but not other stress inducers leads to the disruption of a sub-set of snRNPs and inhibition of in vitro splicing in HeLa cells. EMBO J. 1988; 7(11):3509-18. PMC: 454852. DOI: 10.1002/j.1460-2075.1988.tb03227.x. View

Guthrie C, Patterson B . Spliceosomal snRNAs. Annu Rev Genet. 1988; 22:387-419. DOI: 10.1146/annurev.ge.22.120188.002131. View

Bond U, SCHLESINGER M . The chicken ubiquitin gene contains a heat shock promoter and expresses an unstable mRNA in heat-shocked cells. Mol Cell Biol. 1986; 6(12):4602-10. PMC: 367245. DOI: 10.1128/mcb.6.12.4602-4610.1986. View

Pikielny C, Rymond B, Rosbash M . Electrophoresis of ribonucleoproteins reveals an ordered assembly pathway of yeast splicing complexes. Nature. 1986; 324(6095):341-5. DOI: 10.1038/324341a0. View

Turner B, Franchi L . Identification of protein antigens associated with the nuclear matrix and with clusters of interchromatin granules in both interphase and mitotic cells. J Cell Sci. 1987; 87 ( Pt 2):269-82. DOI: 10.1242/jcs.87.2.269. View

HARDIN J, SPICER S, Greene W . The paranucleolar structure, accessory body of Cajal, sex chromatin, and related structures in nuclei of rat trigeminal neurons: a cytochemical and ultrastructural study. Anat Rec. 1969; 164(4):403-31. DOI: 10.1002/ar.1091640403. View

Spector D, Fu X, Maniatis T . Associations between distinct pre-mRNA splicing components and the cell nucleus. EMBO J. 1991; 10(11):3467-81. PMC: 453075. DOI: 10.1002/j.1460-2075.1991.tb04911.x. View

Rosbash M, Seraphin B . Who's on first? The U1 snRNP-5' splice site interaction and splicing. Trends Biochem Sci. 1991; 16(5):187-90. DOI: 10.1016/0968-0004(91)90073-5. View

Ast G, Goldblatt D, Offen D, Sperling J, Sperling R . A novel splicing factor is an integral component of 200S large nuclear ribonucleoprotein (InRNP) particles. EMBO J. 1991; 10(2):425-32. PMC: 452663. DOI: 10.1002/j.1460-2075.1991.tb07964.x. View

10.

Ruby S, Abelson J . Pre-mRNA splicing in yeast. Trends Genet. 1991; 7(3):79-85. DOI: 10.1016/0168-9525(91)90276-V. View

11.

Andrade L, Chan E, Raska I, Peebles C, Roos G, Tan E . Human autoantibody to a novel protein of the nuclear coiled body: immunological characterization and cDNA cloning of p80-coilin. J Exp Med. 1991; 173(6):1407-19. PMC: 2190846. DOI: 10.1084/jem.173.6.1407. View

12.

Raska I, Andrade L, Ochs R, Chan E, Chang C, Roos G . Immunological and ultrastructural studies of the nuclear coiled body with autoimmune antibodies. Exp Cell Res. 1991; 195(1):27-37. DOI: 10.1016/0014-4827(91)90496-h. View

13.

Raska I, Ochs R, Andrade L, Chan E, Burlingame R, Peebles C . Association between the nucleolus and the coiled body. J Struct Biol. 1990; 104(1-3):120-7. DOI: 10.1016/1047-8477(90)90066-l. View

14.

Spector D . Higher order nuclear organization: three-dimensional distribution of small nuclear ribonucleoprotein particles. Proc Natl Acad Sci U S A. 1990; 87(1):147-51. PMC: 53217. DOI: 10.1073/pnas.87.1.147. View

15.

Fu X, Maniatis T . Factor required for mammalian spliceosome assembly is localized to discrete regions in the nucleus. Nature. 1990; 343(6257):437-41. DOI: 10.1038/343437a0. View

16.

Zieve G, Sauterer R . Cell biology of the snRNP particles. Crit Rev Biochem Mol Biol. 1990; 25(1):1-46. DOI: 10.3109/10409239009090604. View

17.

Krainer A, Conway G, Kozak D . Purification and characterization of pre-mRNA splicing factor SF2 from HeLa cells. Genes Dev. 1990; 4(7):1158-71. DOI: 10.1101/gad.4.7.1158. View

18.

Iribarren A, Sproat B, Neuner P, Sulston I, Ryder U, Lamond A . 2'-O-alkyl oligoribonucleotides as antisense probes. Proc Natl Acad Sci U S A. 1990; 87(19):7747-51. PMC: 54825. DOI: 10.1073/pnas.87.19.7747. View

19.

Luhrmann R, Kastner B, Bach M . Structure of spliceosomal snRNPs and their role in pre-mRNA splicing. Biochim Biophys Acta. 1990; 1087(3):265-92. DOI: 10.1016/0167-4781(90)90001-i. View

20.

Billings P, Allen R, JENSEN F, Hoch S . Anti-RNP monoclonal antibodies derived from a mouse strain with lupus-like autoimmunity. J Immunol. 1982; 128(3):1176-80. View