Sequential Entry of Components of the Gene Expression Machinery into Daughter Nuclei

Overview

Journal Mol Biol Cell

Specialties Cell Biology
Molecular Biology

Date 2003 Mar 13

PMID 12631722

Citations 78

Authors

Kannanganattu V Prasanth

Paula A Sacco-Bubulya

Supriya G Prasanth

David L Spector

Affiliations

Soon will be listed here.

Abstract

In eukaryotic cells, RNA polymerase II (RNA pol II) transcription and pre-mRNA processing are coordinated events. We have addressed how individual components of the transcription and pre-mRNA processing machinery are organized during mitosis and subsequently recruited into the newly formed daughter nuclei. Interestingly, localization studies of numerous RNA pol II transcription and pre-mRNA processing factors revealed a nonrandom and sequential entry of these factors into daughter nuclei after nuclear envelope/lamina formation. The initiation competent form of RNA pol II and general transcription factors appeared in the daughter nuclei simultaneously, but prior to pre-mRNA processing factors, whereas the elongation competent form of RNA pol II was detected even later. The differential entry of these factors rules out the possibility that they are transported as a unitary complex. Telophase nuclei were competent for transcription and pre-mRNA splicing concomitant with the initial entry of the respective factors. In addition, our results revealed a low turnover rate of transcription and pre-mRNA splicing factors during mitosis. We provide evidence to support a model in which the entry of the RNA pol II gene expression machinery into newly forming daughter nuclei is a staged and ordered process.

Citing Articles

Interphase chromosome conformation is specified by distinct folding programs inherited via mitotic chromosomes or through the cytoplasm.

Schooley A, Venev S, Aksenova V, Navarrete E, Dasso M, Dekker J bioRxiv. 2024; .

PMID: 39345587 PMC: 11429855. DOI: 10.1101/2024.09.16.613305.

Behavior of Assembled Promyelocytic Leukemia Nuclear Bodies upon Asymmetric Division in Mouse Oocytes.

Udagawa O, Kato-Udagawa A, Hirano S Int J Mol Sci. 2024; 25(16).

PMID: 39201340 PMC: 11354524. DOI: 10.3390/ijms25168656.

Transcriptional repression across mitosis: mechanisms and functions.

Contreras A, Perea-Resa C Biochem Soc Trans. 2024; 52(1):455-464.

PMID: 38372373 PMC: 10903446. DOI: 10.1042/BST20231071.

Nuclear Phosphoinositides as Key Determinants of Nuclear Functions.

Vidalle M, Sheth B, Fazio A, Marvi M, Leto S, Koufi F Biomolecules. 2023; 13(7).

PMID: 37509085 PMC: 10377365. DOI: 10.3390/biom13071049.

Quantitative super-resolution microscopy reveals the differences in the nanoscale distribution of nuclear phosphatidylinositol 4,5-bisphosphate in human healthy skin and skin warts.

Hoboth P, Sztacho M, Quaas A, Akgul B, Hozak P Front Cell Dev Biol. 2023; 11:1217637.

PMID: 37484912 PMC: 10361526. DOI: 10.3389/fcell.2023.1217637.

References

Colwill K, Feng L, Yeakley J, Gish G, Caceres J, Pawson T . SRPK1 and Clk/Sty protein kinases show distinct substrate specificities for serine/arginine-rich splicing factors. J Biol Chem. 1996; 271(40):24569-75. DOI: 10.1074/jbc.271.40.24569. View

Chen D, Hinkley C, Henry R, Huang S . TBP dynamics in living human cells: constitutive association of TBP with mitotic chromosomes. Mol Biol Cell. 2002; 13(1):276-84. PMC: 65088. DOI: 10.1091/mbc.01-10-0523. View

Bregman D, Du L, van der Zee S, WARREN S . Transcription-dependent redistribution of the large subunit of RNA polymerase II to discrete nuclear domains. J Cell Biol. 1995; 129(2):287-98. PMC: 2199908. DOI: 10.1083/jcb.129.2.287. View

West M, Corden J . Construction and analysis of yeast RNA polymerase II CTD deletion and substitution mutations. Genetics. 1995; 140(4):1223-33. PMC: 1206689. DOI: 10.1093/genetics/140.4.1223. View

Siomi H, Dreyfuss G . A nuclear localization domain in the hnRNP A1 protein. J Cell Biol. 1995; 129(3):551-60. PMC: 2120450. DOI: 10.1083/jcb.129.3.551. View

Allemand E, Dokudovskaya S, Bordonne R, Tazi J . A conserved Drosophila transportin-serine/arginine-rich (SR) protein permits nuclear import of Drosophila SR protein splicing factors and their antagonist repressor splicing factor 1. Mol Biol Cell. 2002; 13(7):2436-47. PMC: 117325. DOI: 10.1091/mbc.e02-02-0102. View

Spector D . Nuclear domains. J Cell Sci. 2001; 114(Pt 16):2891-3. DOI: 10.1242/jcs.114.16.2891. View

Schul W, VAN Driel R, de Jong L . A subset of poly(A) polymerase is concentrated at sites of RNA synthesis and is associated with domains enriched in splicing factors and poly(A) RNA. Exp Cell Res. 1998; 238(1):1-12. DOI: 10.1006/excr.1997.3808. View

Calado A, Carmo-Fonseca M . Localization of poly(A)-binding protein 2 (PABP2) in nuclear speckles is independent of import into the nucleus and requires binding to poly(A) RNA. J Cell Sci. 2000; 113 ( Pt 12):2309-18. DOI: 10.1242/jcs.113.12.2309. View

10.

Larsson S, Charlieu J, Miyagawa K, Engelkamp D, Rassoulzadegan M, Ross A . Subnuclear localization of WT1 in splicing or transcription factor domains is regulated by alternative splicing. Cell. 1995; 81(3):391-401. DOI: 10.1016/0092-8674(95)90392-5. View

11.

Mattaj I, Englmeier L . Nucleocytoplasmic transport: the soluble phase. Annu Rev Biochem. 1998; 67:265-306. DOI: 10.1146/annurev.biochem.67.1.265. View

12.

Thompson N, Steinberg T, Aronson D, Burgess R . Inhibition of in vivo and in vitro transcription by monoclonal antibodies prepared against wheat germ RNA polymerase II that react with the heptapeptide repeat of eukaryotic RNA polymerase II. J Biol Chem. 1989; 264(19):11511-20. View

13.

Ferreira J, Carmo-Fonseca M, Lamond A . Differential interaction of splicing snRNPs with coiled bodies and interchromatin granules during mitosis and assembly of daughter cell nuclei. J Cell Biol. 1994; 126(1):11-23. PMC: 2120090. DOI: 10.1083/jcb.126.1.11. View

14.

Kim E, Du L, Bregman D, WARREN S . Splicing factors associate with hyperphosphorylated RNA polymerase II in the absence of pre-mRNA. J Cell Biol. 1997; 136(1):19-28. PMC: 2132468. DOI: 10.1083/jcb.136.1.19. View

15.

Spector D, Smith H . Redistribution of U-snRNPs during mitosis. Exp Cell Res. 1986; 163(1):87-94. DOI: 10.1016/0014-4827(86)90560-4. View

16.

Howell B, Afar D, Lew J, Douville E, Icely P, Gray D . STY, a tyrosine-phosphorylating enzyme with sequence homology to serine/threonine kinases. Mol Cell Biol. 1991; 11(1):568-72. PMC: 359671. DOI: 10.1128/mcb.11.1.568-572.1991. View

17.

Haraguchi T, Koujin T, Hayakawa T, Kaneda T, Tsutsumi C, Imamoto N . Live fluorescence imaging reveals early recruitment of emerin, LBR, RanBP2, and Nup153 to reforming functional nuclear envelopes. J Cell Sci. 2000; 113 ( Pt 5):779-94. DOI: 10.1242/jcs.113.5.779. View

18.

Reuter R, Appel B, Rinke J, Luhrmann R . Localization and structure of snRNPs during mitosis. Immunofluorescent and biochemical studies. Exp Cell Res. 1985; 159(1):63-79. DOI: 10.1016/s0014-4827(85)80038-0. View

19.

Adam S . Transport pathways of macromolecules between the nucleus and the cytoplasm. Curr Opin Cell Biol. 1999; 11(3):402-6. DOI: 10.1016/S0955-0674(99)80056-8. View

20.

Habets W, Hoet M, de Jong B, van der Kemp A, van Venrooij W . Mapping of B cell epitopes on small nuclear ribonucleoproteins that react with human autoantibodies as well as with experimentally-induced mouse monoclonal antibodies. J Immunol. 1989; 143(8):2560-6. View