DOI: 10.1091/mbc.e08-05-0525. Coilin Is Essential for Cajal Body Organization in<i>Drosophila melanogaster</i>

Coilin Is Essential for Cajal Body Organization inDrosophila melanogaster

10.1091/mbc.e08-05-0525

Crossref journal-article

American Society for Cell Biology (ASCB)

Molecular Biology of the Cell (1076)

Abstract

Cajal bodies (CBs) are nuclear organelles that occur in a variety of organisms, including vertebrates, insects, and plants. They are most often identified with antibodies against the marker protein coilin. Because the amino acid sequence of coilin is not strongly conserved evolutionarily, coilin orthologues have been difficult to recognize by homology search. Here, we report the identification of Drosophila melanogaster coilin and describe its distribution in tissues of the fly. Surprisingly, we found coilin not only in CBs but also in histone locus bodies (HLBs), calling into question the use of coilin as an exclusive marker for CBs. We analyzed two null mutants in the coilin gene and a piggyBac insertion mutant, which leads to specific loss of coilin from the germline. All three mutants are homozygous viable and fertile. Cells that lack coilin also lack distinct foci of other CB markers, including fibrillarin, the survival motor neuron (SMN) protein, U2 small nuclear RNA (snRNA), U5 snRNA, and the small CB-specific (sca) RNA U85. However, HLBs are not obviously affected in coilin-null flies. Thus, coilin is required for normal CB organization in Drosophila but is not essential for viability or production of functional gametes.

Bibliography

Liu, J.-L., Wu, Z., Nizami, Z., Deryusheva, S., Rajendra, T. K., Beumer, K. J., Gao, H., Matera, A. G., Carroll, D., & Gall, J. G. (2009). Coilin Is Essential for Cajal Body Organization inDrosophila melanogaster. Molecular Biology of the Cell, 20(6), 1661â1670.

Authors 10

Ji-Long Liu (first)
Zheng'an Wu (additional)
Zehra Nizami (additional)
Svetlana Deryusheva (additional)
T.K. Rajendra (additional)
Kelly J. Beumer (additional)
Hongjuan Gao (additional)
A. Gregory Matera (additional)
Dana Carroll (additional)
Joseph G. Gall (additional)

References 40 Referenced 117

10.1084/jem.173.6.1407 / J. Exp. Med by Andrade L.E.C. (1991)
10.1002/1521-1878(200009)22:9<861::AID-BIES12>3.0.CO;2-Y / BioEssays by Bellini M. (2000)
10.1091/mbc.9.10.2987
10.1073/pnas.0810475105 / Proc. Natl. Acad. Sci. USA by Beumer K. J. (2008)
10.1038/35087045 / Nat. Cell Biol by Blower M. D. (2001)
10.4161/cc.6344 / Cell Cycle by Bongiorno-Borbone L. (2008)
10.1242/dev.118.2.401 / Development by Brand A. H. (1993)
10.1534/genetics.106.065961 / Genetics by Buszczak M. (2007)
{'key': 'B9', 'first-page': '129', 'volume': '2', 'author': 'Cajal S.R.y.', 'year': '1903', 'journal-title': 'Trab. Lab. Invest. Biol'} / Trab. Lab. Invest. Biol by Cajal S.R.y. (1903)
10.1007/BF00365156 / Chromosoma by Callan H. G. (1991)
10.1146/annurev.cellbio.20.010403.103738 / Annu. Rev. Cell Dev. Biol by Cioce M. (2005)
10.1093/bioinformatics/btg430 / Bioinformatics by Clamp M. (2004)
10.1091/mbc.e05-12-1157
10.1093/emboj/21.11.2746 / Eur. Mol. Biol. Organ. J by Darzacq X. (2002)
10.1073/pnas.92.13.5915 / Proc. Natl. Acad. Sci. USA by Frey M. R. (1995)
10.1146/annurev.cellbio.16.1.273 / Annu. Rev. Cell Dev. Biol by Gall J. G. (2000)
10.1038/nrm1262 / Nat. Rev. Mol. Cell Biol by Gall J. G. (2003)
10.1091/mbc.10.12.4385
10.1007/BF00399128 / Chromosoma by Gall J. G. (1981)
10.1038/195788a0 / Nature by Grace T. D. (1962)
10.1074/jbc.M303763200 / J. Biol. Chem by Ilangovan R. (2003)
10.1093/emboj/cdg187 / Eur. Mol. Biol. Organ. J by Jády B. E. (2003)
10.1073/pnas.78.5.2737 / Proc. Natl. Acad. Sci. USA by Lerner E. A. (1981)
10.1073/pnas.0704977104 / Proc. Natl. Acad. Sci. USA by Liu J.-L. (2007)
10.1007/s10577-006-1062-5 / Chromosome Res by Liu J. L. (2006)
10.1083/jcb.200511038 / J. Cell Biol by Liu J. L. (2006)
10.1016/j.ceb.2006.03.005 / Curr. Opin. Cell Biol by Matera A. G. (2006)
10.1083/jcb.200612107 / J. Cell Biol by Morency E. (2007)
10.1016/j.molcel.2007.04.011 / Mol. Cell by Narita T. (2007)
10.1016/0014-4827(91)90496-H / Exp. Cell Res by Raska I. (1991)
10.1002/art.1780300709 / Arthritis Rheumatism by Reimer G. (1987)
10.1016/S0925-4773(98)00157-9 / Mechanisms Dev by Rorth P. (1998)
10.1091/mbc.12.3.565
10.1242/jcs.00211 / J. Cell Sci by Shpargel K. B. (2003)
10.1093/nar/22.22.4673 / Nucleic Acids Res by Thompson J. D. (1994)
10.1083/jcb.200104083 / J. Cell Biol by Tucker K. E. (2001)
10.1006/jsbi.2000.4234 / J. Struct. Biol by Tucker K. E. (2000)
10.1083/jcb.122.4.767 / J. Cell Biol by Tuma R. S. (1993)
10.1073/pnas.90.13.6257 / Proc. Natl. Acad. Sci. USA by Wu C.-H.H. (1993)
10.1091/mbc.5.10.1119

Dates

Type	When
Created	16 years, 7 months ago (Jan. 21, 2009, 9:36 p.m.)
Deposited	3 years, 10 months ago (Sept. 30, 2021, 5:04 a.m.)
Indexed	2 months ago (June 19, 2025, 7:04 a.m.)
Issued	16 years, 5 months ago (March 15, 2009)
Published	16 years, 5 months ago (March 15, 2009)
Published Print	16 years, 5 months ago (March 15, 2009)

Funders 0

None

BibTeX

@article{Liu_2009, title={Coilin Is Essential for Cajal Body Organization inDrosophila melanogaster}, volume={20}, ISSN={1939-4586}, url={http://dx.doi.org/10.1091/mbc.e08-05-0525}, DOI={10.1091/mbc.e08-05-0525}, number={6}, journal={Molecular Biology of the Cell}, publisher={American Society for Cell Biology (ASCB)}, author={Liu, Ji-Long and Wu, Zheng’an and Nizami, Zehra and Deryusheva, Svetlana and Rajendra, T.K. and Beumer, Kelly J. and Gao, Hongjuan and Matera, A. Gregory and Carroll, Dana and Gall, Joseph G.}, editor={Wickens, Marvin}, year={2009}, month=mar, pages={1661–1670} }

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      "affiliation": []
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  "short-title": [],
  "issued": {
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        15
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  "journal-issue": {
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          15
        ]
      ]
    }
  },
  "alternative-id": [
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  "URL": "http://dx.doi.org/10.1091/mbc.e08-05-0525",
  "relation": {
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  "ISSN": [
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    "1939-4586"
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  "subject": [],
  "container-title-short": "MBoC",
  "published": {
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}