The dynamic nuclear redistribution of an hnRNP K-homologous protein during Drosophila embryo development and heat shock. Flexibility of transcription sites in vivo

Journal of Cell Biology

Volumn 137, Issue 2, 1997, Pages 291-303

  Buchenau, Peter ^a,c   Saumweber, Harald ^b   Arndt Jovin, Donna J ^a  

^a MAX PLANCK INSTITUTE FOR BIOPHYSICAL CHEMISTRY   (Germany)

^b HUMBOLDT UNIVERSITY   (Germany)

^c UNIVERSITY OF BONN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

DNA; NUCLEAR PROTEIN; RNA;

AMINO ACID SEQUENCE; ANIMAL CELL; ARTICLE; CHROMATIN STRUCTURE; COMPLEX FORMATION; DROSOPHILA; EMBRYO; EMBRYO CULTURE; GENETIC TRANSCRIPTION; HEAT SHOCK; NONHUMAN; PRIORITY JOURNAL; SEQUENCE HOMOLOGY; TRANSCRIPTION REGULATION;

ANIMALS; ANTIBODIES, MONOCLONAL; CELL NUCLEUS; DROSOPHILA MELANOGASTER; EMBRYO, NONMAMMALIAN; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HEAT-SHOCK RESPONSE; HETEROGENEOUS-NUCLEAR RIBONUCLEOPROTEIN K; HETEROGENEOUS-NUCLEAR RIBONUCLEOPROTEINS; INTERPHASE; RIBONUCLEOPROTEINS; RNA, MESSENGER; TRANS-ACTIVATION (GENETICS); TRANSCRIPTION, GENETIC;

EID: 0030964113     PISSN: 00219525     EISSN: None     Source Type: Journal    
DOI: 10.1083/jcb.137.2.291     Document Type: Article

References (66)

1. Allis, C.D., G.L. Waring, and A.P. Mahowald. 1977. Mass isolation of pole cells from Drosophila melanogaster. Dev. Biol. 56:372-381.
2. Bendena, W.O., J.C. Garbe, K.L. Traverse, S.C. Lakhotia, and M.L. Pardue. 1989. Multiple inducers of the Drosophila heat shock locus 93D (hsrω): Inducer-specific patterns of the three transcripts. J. Cell Biol. 108:2017-2028.
3. Bendena, W.G., A. Ayme-Southgate, J.C. Garbe, and M.L. Pardue. 1991. Expression of heat-shock locus hsr-omega in nonstressed cells during development in Drosophila melanogaster. Dev. Biol. 144:65-77.
4. Blobel, G. 1985. Gene gating: a hypothesis. Proc. Natl. Acad. Sci. USA. 82: 8527-8529.
5. Bonner, J.J., and M.L. Pardue. 1976. The effect of heat shock on RNA synthesis in Drosophila tissues. Cell. 8:43-50.
6. Buchenau, P. 1996. Verteilung, Funktion und in vivo-Dynamik chromosomaler Proteine in Drosophila melanogaster. Ph.D. thesis. Humboldt University of Berlin, Berlin, Germany.
7. Buchenau, P., D.J. Arndt-Jovin, and H. Saumweber. 1993a. In vivo observation of the puff-specific protein no-on transient A (NONA) in nuclei of Drosophila embryos. J. Cell Sci. 106:189-199.
8. Buchenau, P., H. Saumweber, and D.J. Arndt-Jovin. 1993b. Consequences of topoisomerase II inhibition in early embryogenesis of Drosophila revealed by in vivo confocal laser scanning microscopy. J. Cell Sci. 104:1175-1185.
9. Campos-Ortega, J., and V. Hartenstein. 1985. The Embryonic Development of Drosophila melanogaster. Springer-Verlag Inc., Heidelberg, Germany. 227 pp.
10. Cremer, T., A. Kurz, R. Zirbel, S. Dietzel, B. Rinke, E. Schröck, M. Speicher, U. Mathieu, A. Jauch, P. Emmerich et al. 1994. Role of chromosome territories in the functional compartmentalization of the cell nucleus. Cold Spring Harb. Symp. Quant. Biol. 58:777-792.
11. Dangli, A., and E.K.F. Bautz. 1983. Differential distribution of nonhistone proteins from polytene chromosomes of Drosophila melanogaster after heat shock. Chromosoma (Berlin). 88:201-207.
12. Dangli, A., C. Grond, P. Kloetzel, and E.K.F. Bautz. 1983. Heat-shock puff 93D from Drosophila melanogaster, accumulation of an RNP-specific antigen associated with giant particles of possible storage function. EMBO (Eitr. MoI. Biol. Organ.) J. 2:1747-1751.
13. de Boni, U. 1994. The interphase nucleus as a dynamic structure. Int. Rev. Cytol. 150:149-171.
14. Dequin, R., H. Saumweber, and J.W. Sedat. 1984. Proteins shifting from the cytoplasm into the nuclei during early embryogenesis of Drosophila melanogaster. Dev. Biol. 104:37-48.
15. Dernburg, A.F., K.W. Broman, J.C. Fung, W.F. Marshall, J. Philips, D.A. Agard, and J.W. Sedat. 1996. Perturbation of nuclear architecture by long-distance chromosome interactions. Cell. 85:745-759.
16. Dreyfuss, G., M.J. Matunis, S. Piñol-Roma, and C.G. Burd. 1993. hnRNP proteins and the biogenesis of mRNA. Annu. Rev. Biochem. 62:289-321.
17. Dubochet, J. 1995. High-pressure freezing for cryoelectron microscopy. Trends Cell Biol. 5:366-368.
18. Dworetzky, S.I., K.L. Wright, E.G. Fey, S. Penman, J.B. Lian, J.L. Stein, and G.S. Stein. 1992. Sequence-specific DNA-binding proteins are components of a nuclear matrix-attachment site. Proc. Natl. Acad. Sci. USA. 89:4178-4182.
19. Foe, V., and B. Alberts. 1983. Studies of nuclear and cytoplasmic behavior during the five mitotic cycles that precede gastrulation in Drosophila embryo-genesis. J. Cell Sci. 61:31-70.
20. Garbe, J.C., and M.L. Pardue. 1986. Heat shock locus 93D of Drosophila melanogaster. A spliced RNA most strongly conserved in the intron sequence. Proc. Natl. Acad. Sci. USA. 83:1812-1816.
21. Garbe, J.C., W.G. Bendena, M. Alfano, and M.L. Pardue. 1986. A Drosophila heat shock locus with a rapidly diverging sequence but a conserved structure. J. Biol. Chem. 261:16889-16894.
22. Gemkow, M., P. Buchenau, and D. Arndt-Jovin. 1996. FISH in whole mount Drosophila embryos. RNA: activation of a transcriptional locus: DNA: gene architecture and expression. Bioimaging. 4:107-120.
23. Haynes, S.R., G. Raychaudhuri, and A.L. Beyer. 1990. The Drosophila Hrb98DE locus encodes four protein isoforms homologous to the A1 protein of mammalian heterogeneous nuclear ribonucleoprotein complexes. Mol. Cell. Biol. 10:316-323.
24. Haynes, S.R., D. Johnson, G. Raychaudhuri, and A.L. Beyer. 1991. The Drosophila Hrb87f gene encodes a new member of the A and B hnRNP protein group. Nucleic Acids Res. 19:25-32.
25. He, D., C. Zeng, and B.R. Brinkley. 1995. Nuclear matrix proteins as structural and functional components of the mitotic apparatus. Int. Rev. Cytol. 162B:1-74.
26. Hernandez-Verdun, D., and T. Gautier. 1994. The chromosome periphery during mitosis. Bioessays. 16:179-185.
27. Hiraoka, Y., A.F. Dernburg, S.J. Parmelee, 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.
28. Hogan, N.C., K.L. Traverse, D.E. Sullivan, and M.L. Pardue. 1994. The nucleus-limited Hsr-omega-n transcript is a polyadenylated RNA with a regulated intranuclear turnover. J. Cell Biol. 125:21-30.
29. Hogan, N.C., F. Slot, K.L. Traverse, J.C. Garbe, W.O. Bendena, and M.L. Pardue. 1995. Stability of tandem repeats in the Drosophila melanogaster Hsr-omega nuclear RNA. Genetics. 139:1611-1621.
30. Hovemann, B., U. Walldorf, and R.-P. Ryseck. 1986. Heat-shock locus 93D of Drosophila melanogaster: an RNA with limited coding capacity accumulates precursor transcripts after heat shock. Mol. Gen. Genet. 204:334-340.
31. Hovemann, B.T., E. Dessen, H. Mechler, and E. Mack. 1991. Drosophila snRNP associated protein P11 which specifically binds to heat shock puff 93D reveals strong homology with hnRNP core protein A1. Nucleic Acids Res. 19: 4909-4914.
32. Hutchison, N., and H. Weintraub. 1985. Localization of DNAse I-sensitive sequences to specific regions of interphase nuclei. Cell. 43:471-482.
33. Janevski, J., P. Park, and U. de Boni. 1995. Organization of centromeric domains in hepatocyte nuclei: rearrangement associated with de novo activation of the vitellogenin gene family in Xenopus laevis. Exp. Cell Res. 217: 227-239.
34. Kabisch, R., and E. Bautz. 1983. Differential distribution of RNA polymerase B and nonhistone chromosomal proteins in polytene chromosomes of Drosophila melaogaster. EMBO (Eur. Mol. Biol. Organ.) J. 2:395-402.
35. Kallajoki, M., and M. Osborn. 1994. Gel electrophoretic analysis of nuclear matrix fractions isolated from different human cell lines. Electrophoresis. 15: 520-528.
36. Lakhotia, S.C., and A. Sharma. 1995. RNA metabolism in situ at the 93D heat shock locus in polytene nuclei of Drosophila melanogaster after various treatments. Chromosome Res. 3:151-161.
37. Leffers, H., K. Dejgaard, and J.E. Celis. 1995. Characterisation of two major cellular poly (rC)-binding human proteins, each containing three K-homologous (KH) domains. Eur. J. Biochem. 230:447-453.
38. Lewis, C.D., J.S. Lebkowski, A.K. Daly, and U.K. Laemmli. 1984. Interphase nuclear matrix and metaphase scaffolding structures. J. Cell Sci. Suppl. 1: 103-122.
39. Manuelidis, L., and J. Borden. 1988. Reproducible compartmentalization of individual chromosome domains in human CNS cells revealed by in situ hybridization and three-dimensional reconstruction. Chromosoma (Berlin). 96: 397-410.
40. Mattern, K., B. Humbel, A. Muijsers, L. de Jong, and R. van Driel. 1996. hnRNP proteins and B23 are the major proteins of the internal nuclear matrix of HeLa S3 cells. J. Cell. Biochem. 62:275-289.
41. Matunis, E.L., M.J. Matunis, and O. Dreyfuss. 1992a. Characterization of the major hnRNP proteins from Drosophila melanogaster. J. Cell Biol. 116:257-270.
42. Matunis, M.J., W.M. Michael, and G. Dreyfuss. 1992b. Characterization and primary structure of the poly(C)-binding heterogeneous nuclear ribonucleoprotein complex K protein. Mol. Cell. Biol. 12:164-171.
43. Matunis, E.L., M.J. Matunis, and G. Dreyfuss. 1993. Association of individual hnRNP proteins and snRNPs with nascent transcripts. J. Cell Biol. 121:219-228.
44. Mayeda, A., and A.R. Krainer. 1992. Regulation of alternative pre-mRNA splicing by hnRNP and splicing factor SF2. Cell. 68:365-375.
45. Michelotti, E., G. Michelotti, A. Aronsohn, and D. Levens. 1996. Heterogeneous nuclear ribonucleoprotein K is a transcription factor. Mol. Cell. Biol. 16:2350-2360.
46. Mitchison, T.J., and J.W. Sedat. 1983. Localization of antigenic determinants in whole Drosophila embryos. Dev. Biol. 99:261-264.
47. Morcillo, G., J.L. Diez, M.E. Carbajal, and R.M. Tanguay. 1993. HSP90 associates with specific heat shock puffs (hsr omega) in polytene chromosomes of Drosophila and Chironomus. Chromosoma (Berlin). 102:648-659.
48. Osborn, M., and K. Weber. 1982. Immunofluorescence and immunocytochemical procedures with affinity purified antibodies: tubulin-containing structures. Methods Cell Biol. 24:97-132.
49. Park, P.C., and U. de Boni. 1992. Spatial rearrangement and enhanced clustering of kinetochores in interphase nuclei of dorsal root ganglion neurons in vitro: association with nucleolar fusion. Exp. Cell Res. 203:222-229.
50. Rabl, C. 1885. Über Zellteilung. Morphal. Jahrbuch. 10:214-330.
51. Risau, W., P. Symmons, H. Saumweber, and M. Frasch. 1983. Nonpackaging and packaging proteins of hnRNA in Drosophila melanogaster. Cell. 33: 529-541.
52. Sahlas, D.J., K. Milankov, P.C. Park, and U. de Boni. 1993. Distribution of snRNPs, splicing factor SC-35 and actin in interphase nuclei: immunocytochemical evidence for differential distribution during changes in functional states. J. Cell Sci. 105:347-357.
53. Saumweber, H., P. Symmons, R. Kabisch, H. Will, and F. Bonhoeffer. 1980. Monoclonal antibodies against chromosomal proteins of Drosophila melanogaster. Chromosoma (Berlin). 80:253-275.
54. Schmidt, E.R. 1992. A simplified and efficient protocol for nonradioactive in situ hybridization to polytene chromosomes with a DIG-iabeled DNA probe. In Nonradioactive in situ Hybridization. Application Manual. S. Grünewald-Junho, J. Keesey, M. Leous, M. Miltenburg, and C. Schroeder, editors. Boehringer GmbH Biochemica, Mannheim, Germany. Second Edition. 97-99.
55. Segalat, L., and J.A. Lepesant. 1992. Spatial distribution of the Sm antigen in Drosophila early embryos. Biol. Cell. 75:181-185.
56. Sharma, A., and S.C. Lakhotia. 1995. In situ quantification of hsp70 and alpha-beta transcripts at 87A and 87C loci in relation to hsr-omega gene activity in polytene cells of Drosophila melanogaster. Chromosome Res. 3:386-393.
57. Spector, D., R. O'Keefe, and L. Jimenez-Garcia. 1994. Dynamics of transcription and pre-mRNA splicing within the mammalian cell nucleus. Cold Spring Harbor Symp. Quant. Biol. 58:799-805.
58. Strouboulis, J., and A.P. Wolffe. 1996. Functional compartmentalization of the nucleus. J. Cell Sci. 109:1991-2000.
59. Stuurman, N., L. de Jong, and R. van Driel. 1992. Nuclear frameworks: concepts and operational definitions. Cell Biol. Int. Rep. 16:837-852.
60. Swedlow, J.R., D.A. Agard, and J.W. Sedat. 1993. Chromosome structure inside the nucleus. Curr. Opin. Cell Biol. 5:412-416.
61. van Driel, R., D.G. Wansink, B. van Steensel, M.A. Grande, W. Schul, and L. de Jong. 1995. Nuclear domains and the nuclear matrix. Int. Rev. Cytol. 162A:151-189.
62. Vazquez, J., D. Pauli, and A. Tissieres. 1993. Transcriptional regulation in Drosophila during heat shock: a nuclear run-on analysis. Chromosoma (Berlin). 102:233-248.
63. Wansink, D.G., W. Schul, I. van der Kraan, B. van Steensel, R. van Driel, and L. de Jong. 1993. Fluorescent labeling of nascent RNA reveals transcription by RNA polymerase II in domains scattered throughout the nucleus. J. Cell Biol. 122:283-293.
64. Wansink, D.G., E.E. Manders, I. van der Kraan, J. A. Aten, R. van Driel, and L. de Jong. 1994. RNA polymerase II transcription is concentrated outside replication domains throughout S-phase. J. Cell Sci. 107:1449-1456.
65. Xing, Y., C.V. Johnson, P.R. Dobner, and J.B. Lawrence. 1993. Higher level organization of individual gene transcription and RNA splicing. Science (Wash. DC). 259:1326-1330.
66. Zirbel, R.M., U.R. Mathieu, A. Kurz, T. Cremer, and P. Lichter. 1993. Evidence for a nuclear compartment of transcription and splicing located at chromosome domain boundaries. Chromosome Res. 1:93-106.