The Drosophila melanogaster Cajal body

Journal of Cell Biology

Volumn 172, Issue 6, 2006, Pages 875-884

  Liu, Ji Long ^a   Murphy, Christine ^a   Buszczak, Michael ^a   Clatterbuck, Sarah ^b   Goodman, Robyn ^b   Gall, Joseph G ^a  

^a GEOPHYSICAL LABORATORY   (United States)

^b JOHNS HOPKINS UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FIBRILLARIN; HISTONE; MOLECULAR MOTOR; SMALL NUCLEAR RIBONUCLEOPROTEIN; SMALL NUCLEAR RNA;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL NUCLEUS INCLUSION BODY; CELL ULTRASTRUCTURE; COILED BODY; CONTROLLED STUDY; DROSOPHILA MELANOGASTER; FEMALE; GENE LOCATION; GENE LOCUS; MOLECULAR PROBE; NONHUMAN; NUCLEOLUS; PRIORITY JOURNAL; RNA ANALYSIS; VERTEBRATE;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; CELL NUCLEUS; COILED BODIES; DROSOPHILA MELANOGASTER; EMBRYO, NONMAMMALIAN; EVOLUTION, MOLECULAR; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HISTONES; LARVA; MULTIGENE FAMILY; PROTEIN BIOSYNTHESIS; RIBONUCLEOPROTEIN, U7 SMALL NUCLEAR; RIBONUCLEOPROTEINS, SMALL NUCLEAR; RNA, MESSENGER; SPECIES SPECIFICITY;

ANIMALIA; DROSOPHILA MELANOGASTER; VERTEBRATA;

EID: 33644915790     PISSN: 00219525     EISSN: 00219525     Source Type: Journal    
DOI: 10.1083/jcb.200511038     Document Type: Article

References (74)

1. Alonso, A., J. Jorcano, E. Beck, and E. Spiess. 1983. Isolation and characterization of Drosophila melanogaster U2 small nuclear RNA genes. J. Mol. Biol. 169:691-705.
2. Andrade, L.E.C., E.K.L. Chan, I. Raska, C.L. Peebles, G. Roos, and E.M. Tan. 1991. Human autoantibody to a novel protein of the nuclear coiled body: immunological characterization and cDNA cloning of p80-coilin. J. Exp. Med. 173:1407-1419.
3. Andrade, L.E.C., E.M. Tan, and E.K.L. Chan. 1993. Immunocytochemical analysis of the coiled body in the cell cycle and during cell proliferation. Proc. Natl. Acad. Sci. USA. 90:1947-1951.
4. Azzouz, T.N., and D. Schümperli. 2003. Evolutionary conservation of the U7 small nuclear ribonucleoprotein in Drosophila melanogaster. RNA. 9:1532-1541.
5. Bauer, D.W., 61nd J.G. Gall. 1997. Coiled bodies without coilin. Mol. Biol. Cell. 8:73-82.
6. Bier, K., W. Kunz, and D. Ribbert. 1967. Struktur und Funktion der Oocytenchromosomen und Nukleolen sowie der Extra-DNS während der Oogenese panoistischer und meroistischer Insekten. Chromosoma. 23:214-254.
7. Brand, A.H., and N. Perrimon. 1993. Targeted gene expression as a means of altering fates and generating dominant phenotypes. Development. 118:401-415.
8. Cajal, S.R.y. 1903. Un sencillo metodo de coloracion seletiva del reticulo protoplasmatico y sus efectos en los diversos organos nerviosos de vertebrados e invertebrados. Trabajos del Laboratorio de Investigaciones Biologicas de la Universidad de Madrid. 2:129-221.
9. Callan, H.G., J.G. Gall, and C. Murphy. 1991. Histone genes are located at the sphere loci of Xenopus lampbrush chromosomes. Chromosoma. 101:245-251.
10. Calvi, B.R., M.A. Lilly, and A.C. Spradling. 1998. Cell cycle control of chorion gene amplification. Genes Dev. 12:734-744.
11. Carmo-Fonseca, M. 2002. New clues to the function of the Cajal body. EMBO Rep. 3:726-727.
12. Carmo-Fonseca, M., D. Tollervey, S.M.L. Barabino, A. Merdes, C. Brunner, P.D. Zamore, M.R. Green, E. Hurt, and A.I. Lamond. 1991. Mammalian nuclei contain foci which are highly enriched in components of the pre-mRNA splicing machinery. EMBO J. 10:195-206.
13. Chan, Y.B., I. Miguel-Aliaga, C. Franks, N. Thomas, B. Trulzsch, D.B. Sattelle, K.E. Davies, and M. van den Heuvel. 2003. Neuromuscular defects in a Drosophila survival motor neuron gene mutant. Hum. Mol. Genet. 12:1367-1376.
14. Cioce, M., and A. Lamond. 2005. Cajal bodies: a long history of discovery. Annu. Rev. Cell Dev. Biol. 21:105-131.
15. Darzacq, X., B.E. Jády, C. Verheggen, A.M. Kiss, E. Bertrand, and T. Kiss. 2002. Cajal body-specific small nuclear RNAs: a novel class of 2′-O-methylation and pseudouridylation guide RNAs. EMBO J. 21:2746-2756.
16. Davis, F., T.Y. Tsao, S.K. Fowler, and P.N. Rao. 1983. Monoclonal antibodies to mitotic cells. Proc. Natl. Acad. Sci. USA. 80:2926-2930.
17. Dominski, Z., X.-C. Yang, M. Purdy, and W.F. Marzluff. 2003. Cloning and characterization of the Drosophila U7 small nuclear RNA. Proc. Natl. Acad. Sci. USA. 100:9422-9427.
18. Dominski, Z., X.-C. Yang, and W.F. Marzluff. 2005. The polyadenylation factor CPSF-73 is involved in histone-pre-mRNA processing. Cell. 123:37-48.
19. Frey, M.R., and A.G. Matera. 1995. Coiled bodies contain U7 small nuclear RNA and associate with specific DNA sequences in interphase human cells. Proc. Natl. Acad. Sci. USA. 92:5915-5919.
20. Fung, J.C., W.F. Marshall, A.F. Dernburg, D.A. Agard, and J.W. Sedat. 1998. Homologous chromosome pairing in Drosophila melanogaster proceeds through multiple independent initiations. J. Cell Biol. 141:5-20.
21. Galardi, S., A. Fatica, A. Bachi, A. Scaloni, C. Presutti, and I. Bozzoni. 2002. Purifi ed box C/D snoRNPs are able to reproduce site-specific 2′-Omethylation of target RNA in vitro. Mol. Cell. Biol. 22:6663-6668.
22. Gall, J.G. 1998. In situ hybridization of DNA and nuclear RNA in tissue squashes using 3H-labeled probes. In Cells: A Laboratory Manual, vol. 3. D. Spector, R. Goldman, and L. Leinwand, editors. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY. 114.1-114.11.
23. Gall, J.G. 2000. Cajal bodies: the first 100 years. Annu. Rev. Cell Dev. Biol. 16:273-300.
24. Gall, J.G. 2003. The centennial of the Cajal body. Nat. Rev. Mol. Cell Biol. 4:975-980.
25. Gall, J.G., E.C. Stephenson, H.P. Erba, M.O. Diaz, and G. Barsacchi-Pilone. 1981. Histone genes are located at the sphere loci of newt lampbrush chromosomes. Chromosoma. 84:159-171.
26. Gall, J.G., A. Tsvetkov, Z. Wu, and C. Murphy. 1995. Is the sphere organelle/ coiled body a universal nuclear component? Dev. Genet. 16:25-35.
27. Gall, J.G., M. Bellini, Z. Wu, and C. Murphy. 1999. Assembly of the nuclear transcription and processing machinery: Cajal bodies (coiled bodies) and transcriptosomes. Mol. Biol. Cell. 10:4385-4402.
28. Grace, T.D. 1962. Establishment of four strains of cells from insect tissues grown in vitro. Nature. 195:788-789.
29. Hebert, M.D., P.W. Szymczyk, K.B. Shpargel, and A.G. Matera. 2001. Coilin forms the bridge between Cajal bodies and SMN, the spinal muscular atrophy protein. Genes Dev. 15:2720-2729.
30. Hebert, M.D., K.B. Shpargel, J.K. Ospina, K.E. Tucker, and A.G. Matera. 2002. Coilin methylation regulates nuclear body formation. Dev. Cell. 3:329-337.
31. Hiraoka, Y., A.F. Dernburg, S.J. Parmalee, M.C. Rykowski, D.A. Agard, and J.W. Sedat. 1993. The onset of homologous chromosome pairing during Drosophila melanogaster embryogenesis. J. Cell Biol. 120:591-600.
32. Huang, S., and D.L. Spector. 1992. U1 and U2 small nuclear RNAs are present in nuclear speckles. Proc. Natl. Acad. Sci. USA. 89:305-308.
33. Hulsebos, T.J.M., J.H.P. Hackstein, and W. Hennig. 1984. Lampbrush loop-specific protein of Drosophila hydei. Proc. Natl. Acad. Sci. USA. 81:3404-3408.
34. Ilangovan, R., W.L. Marshall, Y. Hua, and J. Zhou. 2003. Inhibition of apoptosis by Z-VAD-fmk in SMN-depleted S2 cells. J. Biol. Chem. 278:30993-30999.
35. Jády, B.E., and T. Kiss. 2001. A small nucleolar guide RNA functions both in 2'-O-ribose methylation and pseudouridylation of the U5 spliceosomal RNA. EMBO J. 20:541-551.
36. Jády, B.E., X. Darzacq, K.E. Tucker, A.G. Matera, E. Bertrand, and T. Kiss. 2003. Modification of Sm small nuclear RNAs occurs in the nucleoplasmic Cajal body following import from the cytoplasm. EMBO J. 22:1878-1888.
37. Kambach, C., S. Walke, and K. Nagai. 1999. Structure and assembly of the spliceosomal small nuclear ribonucleoprotein particles. Curr. Opin. Struct. Biol. 9:222-230.
38. Kolev, N.G., and J.A. Steitz. 2005. Symplekin and multiple other polyadenylation factors participate in 3′-end maturation of histone mRNAs. Genes Dev. 19:2583-2592.
39. Lerner, E.A., M.R. Lerner, C.A. Janeway, and J.A. Steitz. 1981. Monoclonal antibodies to nucleic acid-containing cellular constituents: Probes for molecular biology and autoimmune disease. Proc. Natl. Acad. Sci. USA. 78:2737-2741.
40. Liu, J.-L., M.D. Hebert, Y. Ye, D.J. Templeton, H.-J. Kung, and A.G. Matera. 2000. Cell cycle-dependent localization of the CDK2-cyclin E complex in Cajal (coiled) bodies. J. Cell Sci. 113:1543-1552.
41. Liu, Q., and G. Dreyfuss. 1996. A novel nuclear structure containing the survival of motor neurons protein. EMBO J. 15:3555-3565.
42. PAT by cyclin E/Cdk2 in Cajal bodies promotes histone gene transcription. Genes Dev. 14:2298-2313.
43. Mahowald, A.P., and M. Tiefert. 1970. Fine structural changes in the Drosophila oocyte nucleus during a short period of RNA synthesis. Wilhelm Roux' Archiv für Entwicklungsmechanik Der Organismen. 165:8-25.
44. Matera, A.G. 2003. Cajal bodies. Curr. Biol. 13:R503.
45. Matera, A.G., and D.C. Ward. 1993. Nucleoplasmic organization of small nuclear ribonucleoproteins in cultured human cells. J. Cell Biol. 121:715-727.
46. Matera, A.G., and M.R. Frey. 1998. Coiled bodies and gems: Janus or Gemini? Am. J. Hum. Genet. 63:317-321.
47. Meister, G., and U. Fischer. 2002. Assisted RNP assembly: SMN and PRMT5 complexes cooperate in the formation of spliceosomal UsnRNPs. EMBO J. 21:5853-5863.
48. Nagai, T., K. Ibata, E.S. Park, M. Kubota, K. Mikoshiba, and A. Miyawaki. 2002. A variant of yellow fl uorescent protein with fast and efficient maturation for cell-biological applications. Nat. Biotechnol. 20:87-90.
49. Ochs, R.L., M.A. Lischwe, W.H. Spohn, and H. Busch. 1985. Fibrillarin: a new protein of the nucleolus identifi ed by autoimmune sera. Biol. Cell. 54:123-134.
50. Pardue, M.L., L.H. Kedes, E.S. Weinberg, and M.L. Birnstiel. 1977. Localization of sequences coding for histone messenger RNA in the chromosomes of Drosophila melanogaster. Chromosoma. 63:135-151.
51. Patel, N. 1994. Imaging neuronal subsets and other cell types in whole-mount Drosophila embryos and larvae using antibody probes. In Drosophila melanogaster: Practical Uses in Cell and Molecular Biology. L.S.B. Goldstein and E.A. Fyrberg, editors. Academic Press, San Diego, CA. 445-487.
52. Pellizzoni, L., J. Yong, and G. Dreyfuss. 2002. Essential role for the SMN complex in the specificity of snRNP assembly. Science. 298:1775-1779.
53. Pillai, R.S., C.L. Will, R. Lührmann, D. Schümperli, and B. Muller. 2001. Purifi ed U7 snRNPs lack the Sm proteins D1 and D2 but contain Lsm10, a new 14 kDa Sm D1-like protein. EMBO J. 20:5470-5479.
54. Pillai, R.S., M. Grimmler, G. Meister, C.L. Will, R. Lührmann, U. Fischer, and D. Schümperli. 2003. Unique Sm core structure of U7 snRNPs: assembly by a specialized SMN complex and the role of a new component, Lsm11, in histone RNA processing. Genes Dev. 17:2321-2333.
55. Raska, I., L.E.C. Andrade, R.L. Ochs, E.K.L. Chan, C.-M. Chang, G. Roos, and E.M. Tan. 1991. Immunological and ultrastructural studies of the nuclear coiled body with autoimmune antibodies. Exp. Cell Res. 195:27-37.
56. r 34,000 nucleolar protein of the U3 RNP particle. Arthritis Rheum. 30:793-800.
57. Richard, P., X. Darzacq, E. Bertrand, B.E. Jády, C. Verheggen, and T. Kiss. 2003. A common sequence motif determines the Cajal body-specific localisation of box H/ACA scaRNAs. EMBO J. 22:4283-4293.
58. Rorth, P. 1998. Gal4 in the Drosophila female germline. Mech. Dev. 78:113-118.
59. Rubin, G.M., L. Hong, P. Brokstein, M. Evans-Holm, E. Frise, M. Stapleton, and D.A. Harvey. 2000. A Drosophila complementary DNA resource. Science. 287:2222-2224.
60. Schaffert, N., M. Hossbach, R. Heintzmann, T. Achsel, and R. Lührmann. 2004. RNAi knockdown of hPrp31 leads to an accumulation of U4/U6 di-snRNPs in Cajal bodies. EMBO J. 23:3000-3009.
61. Schul, W., B. Groenhaut, K. Koberna, Y. Takagaki, A. Jenny, E.M.M. Manders, I. Raska, R. van Driel, and L. de Jong. 1996. The RNA 3′ cleavage factors CstF 64 kDa and CPSF 100 kDa are concentrated in nuclear domains closely associated with coiled bodies and newly synthesized RNA. EMBO J. 15:2883-2892.
62. Schul, W., L. de Jong, and R. van Driel. 1998. Nuclear neighbours: the spatial and functional organization of genes and nuclear domains. J. Cell. Biochem. 70:159-171.
63. Schul, W., I. van der Kraan, A.G. Matera, R. van Driel, and L. de Jong. 1999. Nuclear domains enriched in RNA 3′ processing factors associate with coiled bodies and histone genes in a cell cycle-dependent fashion. Mol. Biol. Cell. 10:3815-3824.
64. Shopland, L.S., M. Byron, J.L. Stein, J.B. Lian, G.S. Stein, and J.B. Lawrence. 2001. Replication-dependent histone gene expression is related to Cajal body (CB) association but does not require sustained CB contact. Mol. Biol. Cell. 12:565-576.
65. Singer, T., and E. Burke. 2003. High-throughput TAIL-PCR as a tool to identify DNA fl anking insertions. Methods Mol. Biol. 236:241-271.
66. Stanek, D., and K.M. Neugebauer. 2004. Detection of snRNP assembly intermediates in Cajal bodies by fl uorescence resonance energy transfer. J. Cell Biol. 166:1015-1025.
67. Tucker, K.E., M.T. Berciano, E.Y. Jacobs, D.F. LePage, K.B. Shpargel, J.J. Rossire, E.K.L. Chan, M. Lafarga, R.A. Conlon, and A.G. Matera. 2001. Residual Cajal bodies in coilin knockout mice fail to recruit Sm sn-RNPs and SMN, the spinal muscular atrophy gene product. J. Cell Biol. 154:293-307.
68. Tucker, K.E., L.K. Massello, L. Gao, T.J. Barber, M.D. Hebert, E.K.L. Chan, and A.G. Matera. 2000. Structure and characterization of the murine p80 coilin gene, Coil. J. Struct. Biol. 129:269-277.
69. Tuma, R.S., J.A. Stolk, and M.B. Roth. 1993. Identification and characterization of a sphere organelle protein. J. Cell Biol. 122:767-773.
70. Wallace, R.A., D.W. Jared, J.N. Dumont, and M.W. Sega. 1973. Protein incorporation by isolated amphibian oocytes: III. Optimum incubation conditions. J. Exp. Zool. 184:321-333.
71. Wu, C.-H.H., and J.G. Gall. 1993. U7 small nuclear RNA in C snurposomes of the Xenopus germinal vesicle. Proc. Natl. Acad. Sci. USA. 90:6257-6259.
72. Yannoni, Y.M., and K. White. 1997. Association of the neuron-specific RNA binding domain-containing protein ELAV with the coiled body in Drosophila neurons. Chromosoma. 105:332-341.
73. Young, P.J., T.T. Le, N.T. Man, A.H.M. Burghes, and G.E. Morris. 2000. The relationship between SMN, the spinal muscular atrophy protein, and nuclear coiled bodies in differentiated tissues and cultured cells. Exp. Cell Res. 256:365-374.
74. Young, P.J., T.T. Le, M. Dunckley, N.T. Man, A.H.M. Burghes, and G.E. Morris. 2001. Nuclear gems and Cajal (coiled) bodies in fetal tissues: nucleolar distribution of the spinal muscular atrophy protein, SMN. Exp. Cell Res. 265:252-261.